HMW 3 - Family text: Callitrichidae (Marmosets and Tamarins)

Text de família: 

Class Mammalia
Order Primates
Suborder Haplorrhini
Infraorder Platyrrhini

  • Small, arboreal monkeys, with colorful tufts, mustaches, fringes, manes, and long non-prehensile tails; they have claw-like nails on all digits except the big toe and two rather than three molar teeth in each quadrant of the jaw; all but one species have twins.
  • 27–74 cm.
  • Neotropical Region, from Panama to south-eastern Brazil and northern Paraguay.
  • Humid submontane and lowland tropical forests, dry semi-deciduous and deciduous forests, gallery forests, and Chacoan forest and scrub.
  • 7 genera, 47 species, 62 taxa.
  • 2 species Critically Endangered, 6 species Endangered, 6 species Vulnerable; none Extinct since 1600.

Marmosets and tamarins have long been recognized as a highly distinct radiation of small, arboreal insectivore-frugivores. The New World monkeys belong to the parvorder Platyrrhini and are distinct from the Old World monkeys or Catarrhini by having three rather than two premolar teeth in each quadrant of the jaw, a tympanic bone that is joined to the side of the auditory bulla but does not extend laterally as a bony tube as it does in catarrhines (both features considered primitive), and large oval nostrils (nares) directed laterally, separated by a broad internarial septum in all but the night monkeys (Aotus) and muriquis (Brachyteles). The predominant classification of the Platyrrhini during the 20th century recognized just two families: Callitrichidae (until the 1950s called the Hapalidae) and Cebidae, the remaining New World monkeys. This division was based on four principal distinguishing features of species of Callitrichidae: their small size (smaller than any of the cebids); claw-shaped nails on all digits except for the big toe (they are sometimes referred to as the “clawed New World monkeys”); two, rather than three, molar teeth on either side of each jaw; and their propensity to give birth to twins. All cebids have nails, have three molar teeth, and generally give birth to single offspring. Callitrichids also lack a hypocone (a rear inner cusp of the crown) on the upper molars, typical of other primates.
In the past, Callitrichidae comprised a logical and coherent grouping of four genera of the smallest New World monkeys, and Cebidae had a mix of seven subfamilies—Saimiriinae, Aotinae, Callicebinae, Pitheciinae, Cebinae, Alouattinae, and Atelinae—and elevengenera. In 1980/1981, this lop-sided division was disputed by A. Rosenberger, who proposed an alternative classification based on phylogenetic relationships and a new scenario of their adaptive radiation. He redefined Cebidae to include two subfamilies, Cebinae with extant genera Cebus and Saimiri, and Callitrichinae (extant genera Callithrix [that included the Pygmy Marmoset, Cebuella pygmaea], Saguinus, Leontopithecus, and Callimico), and he placed all other platyrrhines into a second family, Atelidae. Subsequent molecular genetic phylogenies, notably those produced by H. Schneider and colleagues,largely confirmed Rosenberger’s hypothesis (based on morphology), and, relevant here, clearly aligned marmosets and tamarins with capuchin monkeys (Cebus) and squirrel monkeys (Saimiri). Some authors, notably C. P. Groves, agree with Rosenberger’s and Schneider’s arguments that marmosets and tamarins should be classified as a subfamily, Callitrichinae, to express their close phylogenetic affinity with Cebus and Saimiri (Cebinae), together making up the family Cebidae. Here, however, we maintain them as separate families.
Callitrichids up to this time, as espoused by P. Hershkovitz in his major monograph of 1977, were believed to comprise four genera: the Pygmy Marmoset (Cebuella) in Amazonia; “true” marmosets (Callithrix) in Amazonia and the Atlantic forest of Brazil; lion tamarins (Leontopithecus) also of the Atlantic forest; and tamarins (Saguinus) of the Amazon Basin, Guianas, northern Colombia, and Panama. The division of “marmosets” (Cebuella and Callithrix) and “tamarins” (Saguinus and Leontopithecus) was fixed by W. C. Osman Hill in his treatise of 1957, associating the two common names with two distinct dentitions. The first, belonging to the marmosets, was the “short-tusked” condition, with cylindrical lower incisors elongated to the height of the canines (making the canines appear short), and the second, belonging to the tamarins and lion tamarins, was the “long-tusked” condition, with spatulate incisors and a normal incisor-canine relationship (canines being prominent). This systematic arrangement has been modified over the past years as a result of a better understanding of the phylogenetic relationships among marmosets (Pygmy Marmosets, Amazonian marmosets, and Atlantic forest marmosets) and between marmosets and Goeldi’s Monkey (Callimico goeldii), and with the discovery in 1996 of an entirely new marmoset genus, the dwarf marmoset, Callibella.
Goeldi’s Monkeyhas caused much debate because it has a mix of the four principal features used to define species of Callitrichidae on the one hand and the remaining platyrrhines on the other—it is small and has claws (tegulae), but has single offspring not twins and has three, not two, molar teeth. The first upper molar (M¹) has a small hypocone, and the third molar in Callimico is much reduced in size. P. Hershkovitz believed that traits of Callimico were parallelisms correlated with size and that Goeldi’s Monkey was a relatively primitive (basal) platyrrhine, neither a cebid or a callitrichid or a link between the two; thus, he placed it in its own family, Callimiconidae (as did Osman Hill). This was underpinned by his belief that marmosets and tamarins formed a platyrrhine radiation independent of Callimico and all other New World monkeys. Other authors, inferring that Goeldi’s Monkey might be a primitive callitrichid, placed it in a separate subfamily of Callitrichidae. Rosenberger considered it to be a primitive callitrichine and placed it in its own tribe, Callimiconini. Immunological studies from 1978 (their significance ignored at the time) and genetic evidence from 1989 have shown, however, that Callimico is a sister group to marmosets (Callithrix and Cebuella). Callimico is more closely related to marmosets than are marmosets to tamarins, Saguinus, and lion tamarins (Leontopithecus). Goeldi’s Monkey is now known to be part of the callitrichid radiation even though it has a very small third molar and gives birth to single offspring. Lack of the third molar in callitrichids is believed to be a result of their gradual reduction in size from a larger ancestor—an evolutionary process known as phyletic dwarfism. If all current genera have undergone (or are undergoing) this size reduction at slightly different rates with varying allometry (changing size and shape relationships of the various parts of the body during ontogeny or phylogeny), it is reasonable to believe that Callimico is merely the one genus that has not quite lost the tooth, which is now very small and is described as peg-like and non-functional. The fact that Goeldi’s Monkey produces a single offspring rather than twins is more complicated to rationalizein evolutionary terms. If twinning is an ancestral condition of all callitrichids (and evidently a derived condition in the haplorrhine primates in that no others regularly twin), then it would seem that the ancestral Callimico reverted from twinning to again producing single offspring. The alternative hypothesis is that marmosets and tamarins evolved the habit of twinning independently. The fact that Callimico,like other callitrichids, has a post-partum estrus and delayed embryonic development (1–2 months following conception)—traits that are unique among primates—indicates that the hypothesis that Callimico used to have twins but does not do so today is correct, but the reasons why this should have happened are still unclear.
A small marmoset was discovered on the west bank of the lower Rio Aripuanã in the Amazon in 1996 and was described as Callithrix humilis by M. G. M. van Roosmalen, T. van Roosmalen, R. A. Mittermeier and G. A. B. da Fonseca in 1998. It weighs 150–185 g as an adult and is larger than the Pygmy Marmoset (maximum 140 g) but smaller than all other marmosets (300–400 g). Subsequent morphometric and genetic analyses suggested its classification as a distinct genus Callibella, described byvan Roosmalen and van Roosmalen in 2003, and now the species is named the Black-crowned Dwarf Marmoset (Callibella humilis).
Morphological studies of Rosenberger and a number of molecular genetic studies have demonstrated a close phylogenetic affinity of the Pygmy Marmoset with Amazonian marmosets. This affinity by itself would suggest that they be placed in the same genus, but of further significance is that the Pygmy Marmoset is more closely related to Amazonian marmosets (the argentata group as defined Hershkovitz in 1977) than Amazonian marmosets are to Atlantic forest marmosets (the jacchus group of Hershkovitz). Likewise, Callibella evidently branched off an Amazonian marmoset stem prior to Cebuella and the Amazonian, argentata group of marmosets. This means that recognizing Cebuella and Callibella as distinct genera would make the genus Callithrix paraphyletic—in essence, a problem of having Atlantic forest and Amazonian marmosets that are in the same genus being more different (genetically distant) from each other than are the Black-crowned Dwarf and Pygmy marmosets and Amazonian marmosets that are in different genera. To resolve this, either all pygmy, dwarf, Amazonian and Atlantic forest marmosets must be included in the same genus (a classification espoused by Rosenberger and Groves) or each must be placed in distinct genera. Here, we use the second solution and continue to recognize the Pygmy and Black-crowned Dwarf marmosets as distinct genera, while placing the Amazonian argentata group of marmosets in the genus Mico proposed by Lesson in 1840, to distinguish them from Atlantic forest marmosets (Callithrix). Mico is the oldest generic name applicable to the Amazonian marmosets alone (the type species is the Silvery Marmoset, Mico argentatus). Adopting the first solution, Groves, in his book Primate Taxonomy published in 2001, placed all marmosets in the genus Callithrix, with Cebuella, Callibella, Mico, and Callithrix as subgenera to maintain their distinctions while emphasizing their closeness.
As genera, Saguinus and Leontopithecus have remained stable in recent years, changes occurring only at the level of species and subspecies. In our treatment, therefore, Callitrichidae consists of seven distinct genera: Cebuella (the Pygmy Marmoset), Callibella (the Black-crowned Dwarf Marmoset), Mico (Amazonian marmosets), Callimico (Goeldi’s Monkey), Callithrix (Atlantic forest marmosets), Saguinus (tamarins), and Leontopithecus (lion tamarins).
Hershkovitz’s 1977 revision and synthesis of Callitrichidae recognized 15 species and 45 taxa (species and subspecies). Here, we recognize 47 species and 62 taxa. This increase in the taxonomic diversity of this family has various causes, arising from the discovery of new taxa and taxonomic revisions that have improved on old methods (for example, larger sample sizes, improved techniques for measurement) or used new methods, most notably cytogenetics (studies of chromosome morphology) and molecular analyses of nuclear and mitochondrial genes, facilitated by the ability to use tissue and fecal samples, not just blood. Conceptual changes as to what is considered a species or subspecies also have been involved.
The major taxonomic changes, genus by genus, can be summarized as follows. Hershkovitz considered the Pygmy Marmoset to be monotypic, although two subspecies have been recognized in the past. It is the smallest of the monkeys and has a very wide distribution through the upper (western) Amazon Basin. Considering its enormous range, it would seem likely that there is as-yet-unrecognized diversity, and we choose to maintain the two subspecies to encourage further research. Overall, Hershkovitz placed all “true marmosets” or “ouistitis” known to him in two species groups, comprising just three species: the Callithrix jacchus group (all with ear tufts) of the Atlantic forest and central savanna (Cerrado) of Brazil, with five subspecies, and the C. argentata group of the Amazon, with two species—C. argentata (three subspecies, without ear tufts) and C. humeralifer (also with three subspecies, with ear tufts). We list all jacchus group marmosets as species and recognize Wied’s Black-tufted-ear Marmoset (Callithrix kuhlii), which Hershkovitz believed to be a hybrid. Genetically, it is close to the Black-tufted-ear Marmoset (Callithrix penicillata), but it is consistent in certain differences of its vocalizations and pelage, it has a discrete range in the south of the state of Bahia, and it occupies a distinct habitat. The argentata group has increased in number since 1977 with the description of seven species from the interfluvium of the rios Madeira and Tapajós, some of which Hershkovitz knew of but considered variants of C. argentata melanura. We consider all argentata group marmosets, including the subspecies recognized by Hershkovitz, to be full species, all of them described since 1992. The new species are: Rondon’s Marmoset (Mico rondoni), the Black-headed Marmoset (Mico nigriceps), the Sateré Marmoset (Mico saterei), the Rio Acarí Marmoset (Mico acariensis), the Rio Manicoré Marmoset (Mico manicorensis), the Maués Marmoset (Mico mauesi), and Marca’s Marmoset (Mico marcai)—the last known only from its type locality at the mouth of the Rio Roosevelt. We also list Snethlage’s Marmoset (Mico emiliae), which Hershkovitz regarded as a dark form of C. a. argentata. The marmosets in the southern state of Pará and northern Mato Grosso in Brazil are poorly known.
Hershkovitz’s geographic separation of the Amazonian true marmosets of a tufted-ear and ring-tailed Callithrix humeralifer group (west of the lower Rio Tapajós to the rios Roosevelt and Aripuanã and including subspecies intermedius and chrysoleucus) and a bare-eared C.argentata group (east of the Rio Tapajós and including subspecies leucippe and melanura) is confused now with the presence of the bare-eared and black-tailed form saterei north of the range of intermedius and squeezed between the distributions of the tufted humeralifer and chrysoleucus. The predominance of the diversely tufted-ear forms between the middle and lower rios Tapajós and Madeira is still evident (acariensis, mauesi, humeralifer, chrysoleucus, and intermedius). Those occurring east of the Tapajós and in the south are bare-eared, with no tufts from the middle of the periphery of the ear.
The true marmosets in Amazonia are restricted to the east of the Rio Madeira and south of the Rio Amazonas. The remainder of the Amazon Basin is occupied by tamarins, Saguinus. The diversity recorded by Hershkovitz in 1977 is basically that what is recognized today. Four additions have been made: two new subspecies—“Hernández-Camacho’s Black-mantled Tamarin” (S. nigricollis hernandezi) from Colombia (described by Hershkovitz in 1982) and the “Gray-fronted Saddle-back Tamarin” (S. fuscicollis mura) from between the lower rios Purus and Madeira—and the resurrection of two subspecies (not considered valid taxa by Hershkovitz in 1977)—the “Bearded Emperor Tamarin” (S. imperator subgrisescens) from the upper rios Purus and Juruá and “Gray’s Red-bellied Tamarin” (S. labiatus rufiventer) from between the lower rios Purús and Madeira. A loss was the finding that the “Acre Saddle-back Tamarin” (S. fuscicollis acrensis) recognized by Hershkovitz was in fact a hybrid of the “White Saddle-back Tamarin” (S. weddelli melanoleucus) × Spix’s Saddle-back Tamarin(S. fuscicollis). “Crandall’s Saddle-back Tamarin” (S. weddelli crandalli), known only from a zoo animal, may also prove to be a hybrid; it has never been found in the wild. Major changes to the taxonomy of tamarins have involved the elevation of a number of Hershkovitz’s subspecies to species. There are suggestions, pending further research, that Black-handed Tamarins (Saguinus niger) on either side of the Rio Tocantins are distinct. In 1922, O. Thomas described Mystax ursulus umbratus from Cametá, west of the Rio Tocantins, Pará, but it was considered by Hershkovitz to be a junior synonym. Recent molecular genetic studies have indicated it may in fact be a valid taxon.
The lion tamarins (Leontopithecus) include four species because their distributions today are widely separated and they have distinctive and consistent differences in their pelage coloration and morphology, particularly their dentition and cranium. Genetically, however, they are very similar, and their differentiation is believed to have been recent. It is possible to argue that remnant populations of the four species are now so widely separated because of widespread extinction following the destruction of their lowland forests. Nevertheless, the historical existence of lion tamarins in the state of Espírito Santo, separating the ranges of the Golden Lion Tamarin, Leontopithecus rosalia (Rio de Janeiro) and the Golden-headed Lion Tamarin, Leontopithecus chrysomelas (Bahia), for example, has never been substantiated, and the indications are that they result from populations isolated in forest refuges during the Pleistocene or even the late Tertiary.
Morphological Aspects
The principal distinguishing features of Callitrichidae are their small size (110–700 g; smaller than the smallest cebid, the squirrel monkey, Saimiri, that weighs about 800 g); possession of laterally compressed, sharp, claw-shaped nails (called tegulae) on all the digits except for the big toe (hallux); two, as opposed to three, molar teeth on either side of each jaw (the ancestral condition in placental mammals is three molar teeth); and the propensity to give birth to fraternal (dizygotic) twins. Their upper molar teeth are tritubercular (three cusps forming a triangle) and lack hypocones (a fourth, rear inner cusp of the crown) found in other primates.
Callitrichids have skeletons with relatively long trunks, long non-prehensile tails, and long legs. The forelimbs are shorter than the hindlimbs. The hands and feet are elongated, most particularly in saddle-back tamarins and lion tamarins, the thumb (pollex) is not opposable, and the big toe is small. The head is dolicocephalic, with an ovoid cranium and the brain case being antero-posteriorly elongated and narrowed transversely. The nose is typically platyrrhine, with a broad internarial septum and divergent, laterally projected, oval nostrils. They have small vibrissae on the lips and muzzle, supraorbital area (above the eyes), and forearm. Chief characteristics of the callitrichids are the presence of crests, tufts in and around the ears, manes, mustaches and beards in the various species. The Cotton-top Tamarin (Saguinus oedipus) with its vertical white crest on the crown that turns into a mane and the Emperor Tamarin (Saguinus imperator) with its long mustaches and small beard represent extremes in these aspects. Callitrichids have large ears, which are naked in some species and tufted on or around the ears in other species. The Common Marmoset (Callithrix jacchus) has an “aural corolla”—long white hairs projecting like a fan from around the otherwise naked ear. Ears of the Buffy-tufted-ear Marmoset (Callithrix aurita), the Santarém Marmoset (Mico humeralifer), and the Maués Marmoset have hairs forming prominent tufts from around the pinna and inside the ear (auricle). The skin pigment is usually black, but in a number species the face is pink (for example, Snethlage’s, Rondon’s, and Rio Aripuanã marmosets) or blotchily depigmented pink (for example, the Mottled-face tamarin, Saguinus inustus, and a number of Amazonian marmosets, Mico).
The principal features that define callitrichids are now believed to be derived rather than primitive, and the result of an evolutionary process called phyletic dwarfism, a trend of gradually getting smaller—a secondary reduction in body size. All callitrichids (except Callimico) usually give birth to twins—the only monkeys to do so. This characteristics is inconsistent with their possession of a simplex or unicornuate uterus and only one pair of teats—traits that are typical of the simian primates and believed to be a morphological adaptation to accommodate a single fetus. Because monkeys generally give birth to single offspring, the implication here is that callitrichid twinning is derived and possibly a result of selection to increase their reproductive rate as they get smaller (and hence liable to suffer increased predation). There are other aspects of their reproductive physiology that are unique even among mammals and indicate selection for an augmented reproductive rate, not only in response to increased predation pressure but also as a correlate to their colonization of relatively ephemeral early to mid-successional forests to which they are adapted.
Loss of the third molar, a character of all callitrichids except Callimico, is a result of allometric shortening of the jaw—a shrinking of the mandible and cranium without an equivalent reduction in tooth size. The reduction in the cheek tooth row occurred as an adaptation to balance the molar and premolar occlusal area against reduced body size. Smaller primates tend to have less complex molars. Callimico has a third molar, but it is very small. The morphology of the molars of Callimico is intermediate between marmosets and squirrel monkeys (Saimiri), which also have small third molars. The evolution of claw-like nails also is associated with their small size and their use of broad vertical supports (tree trunks and major limbs) during locomotion and feeding. This is particularly important to marmosets that gouge trees and feed on the gum and to saddle-back tamarins in their particular mode of preying on insects on tree trunks. Larger eyes than would be expect from their orbital aperture are another morphological character that indicates phyletic dwarfism among callitrichids.
Morphological adaptations of marmosets associated with tree gouging and gum feeding include in their teeth, mandibular articulation, jaw-muscle fiber architecture, and large intestine. The action of gouging in these species involves them fixing the anterior dentition of the upper jaw into the bark and gouging upward using their wedge-like, robust, and procumbent lower dentition. Marmoset incisors have thickened labial enamel and lack lingual enamel. Unequal wear of the teeth results in a chisel-like structure. Marmosets have been referred to as “short tusked”; lower incisors are elongated and lower canines are reduced in size relative to the remainder of the anterior teeth, so that the tips of canine teeth are level with the other teeth. Tamarins have tusk-like canines that are longer than their incisors, similar to squirrel monkeys, and they are sometimes termed “long tusked.” The histology of the marmoset’s tooth enamel also shows adaptations to the so-called “increased loading” of the mechanical demands on the teeth from gouging sometimes very hard bark. Enamel is made up of prisms, or cylindrical bundles of enamel called crystalites. In primitive small mammals with soft, undemanding diets, these prisms radiate out uniformly from the dentine layer of the tooth to the surface of the enamel. In larger mammals and those with diets that require strong teeth, the prisms crisscross and undulate. This is known as decussating, and it has the effect of limiting the spread of cracks—a spreading crack will stop when it meets prisms in a different orientation. Cracks in a tooth without this decussation can spread straight to the junction of the enamel and dentine. Callitrichids are unusual for small mammals in that they all have some degree of decussation of the enamel of the anterior dentition; marmosets show more decussation, and often more organized, than tamarins. The closely related and rather larger squirrel monkeys lack decussation of the enamel. In marmosets, the tempero-mandibular joint and shape of the ascending ramus of the lower mandible (where the temporalis muscle is fixed) affect muscle positioning and provide them with the capacity for a very wide gape, which optimizes the angle of the lower jaw and anterior teeth for gouging. The morphology of tendons and muscles of the tempero-mandibular joint (masseter and temporalis muscles) also show specific adaptations for this wide gape. In marmosets, these muscles are relatively large compared with tamarins, and in Common Marmosets, they have longer fibersrelative to their mass, favoringthe ability to stretch in a wider gape. While favoringa wide and forceful gape, these adaptations do not increase bite forces overall, indicating that adaptations involve the need to score the bark rather than gouging it forcefully by biting. Marmosets do bite and pull at fibrous holes in softer bark such as that of Inga (Fabaceae) that provides gum for a number of species.
Callitrichids also have morphological adaptations for fermentation and digestion of tree gum. The Common Marmoset, the Black-headed Marmoset, and Rondon’s Marmoset have large caecums compared with tamarins (Black-handed, Red-bellied, and Weddell’s Saddle-back) and lion tamarins (Golden-headed and Golden). Externally, marmosets’ caecums have deep grooves and ribbons of smooth muscle (taeniae), whereas those of tamarins and the Golden Lion Tamarin are smooth and that of the Golden-headed Lion Tamarin is only lightly grooved. Gut dimensions of tamarins and lion tamarins are typical of primate frugivores, but those of marmosets are more like those of gum-eating prosimians, with relatively short small intestines and larger colons and caecums. The interior of the marmoset’s larger caecum is complex, with folds and sacculations. The caecum acts as a fermentation chamber for the gum and a reservoir for microbial flora, and it is protected from the passage of some digesta, particularly large seeds that tend to be expelled quickly.
Callitrichids occur widely from about 11° N to 25° S, implying that they can occupy a variety of habitats. The northernmost species are tamarins. The White-footed Tamarin (Saguinus leucopus), the Cotton-top Tamarin, and Geoffroy’s Tamarin (Saguinus geoffroyi) occupy humid lowland submontane forest and dry forest in northern Colombia and Panama. Hernández-Camacho’s Black Mantle Tamarin occurs in dry forest in the far north of its range, near La Macarena, Colombia. The Pygmy Marmoset (Cebuella), the Dwarf Marmoset (Callibella), Goeldi’s Monkey (Callimico), all but one of the Amazonian marmosets (Mico), and all tamarins (Saguinus) except for those mentioned above are restricted to forests of the alluvial plains of the Rio Amazonas-Solimões, the Brazilian Shield to the south and Guiana Shield to the north, with some extending into the submontane and montane forests of the Andes at elevations up to 1400 m.
The Pygmy Marmoset is a habitat specialist, occupying lowland forest near, or in, periodically inundated river floodplains; areas where the flood level does not exceed 2–3 m and floods last no longer than three months per year. It reaches its highest densities in these areas but can also occur on higher ground (“terra firma”) in bamboo thickets, liana forest, secondary growth at the edges of pasture and orchards, and tree falls. The limiting resources for this small carnivore-exudativore are an abundance of insects in a very small area (their homes ranges are generally less than 1 ha) and the presence of a principal tree and a number of secondary trees or lianas that provide gums. It is quite probable that seasonal insect migrations and movements caused by flooding are a key attraction of these inundated forests. Very little is known of the ecology and behavior of the Black-crowned Dwarf Marmoset, but the few observations have been made in disturbed primary forest and secondary terra firma forest near plantations, fields, and tree gardens. They have also been seen in riparian forest and seasonally inundated black-water forest (“igapó”).They are believed be gum-feeding specialists similar to, if perhaps not as extreme as, the Pygmy Marmoset. They are slightly larger and perhaps have larger home ranges and a more frugivorous diet than the Pygmy Marmoset and occupy densely vegetated successional forest and forest edge.
The little known Goeldi’s Monkeywas considered, for many years, a habitat specialist of the Amazonian bamboo forest—an open transition forest of limited distribution in the upper Amazon Basin. In these forests, species of bamboo are abundant and even reach the canopy at 30 m, spreading to a crown of up to 10 m in diameter. The bamboos, Merostachys and Bambusa (Guadua), form very dense thickets in the understory. The forest canopy is uneven and broken, encouraging dense understory vegetation of bamboos or other pioneer shrubs, lianas, and small trees growing in the mosaic patches of secondary succession. Bamboo thickets are especially abundant in openings along stream and river banks and in clearings. One of the early field researchers studying the range and habitat of Callimico, K. Izawa, referred to these forests with dense undergrowth as “monte bajo” or “shabby” forests, with patches of “barbecho tupido” (early secondary succession with typical pioneer trees such as Cecropia and Pourouma—both Cecropiacae). Pygmy Marmosets also occur in these forests but always near the river edge. Izawa, attempting to explain the correspondence of the geographical range of Callimico with that of the bamboo forests—both forming an arc from the Río Caquetá in Colombia around the western Amazon through south-eastern Peru and into northern Bolivia (Department of Pando) to the upper Madeira in Brazil—indicated that the shabby forests may have been the predominant vegetation surrounding the enormous Amazonian lake believed to have occurred there in the Tertiary. The major long-term field study of the Pygmy Marmoset by L. Porter found that a Callimico group with a home range of nearly 150 ha spent 76% of its time in the primary forest with a dense understory (monte bajo) and 18–20% its time in bamboo thickets, stream edge, and secondary forest, nearly always traveling, foraging, and feeding at heights averaging 4 m above the ground. The Pygmy Marmoset has exceptional leaping abilities, with long legs compared with tamarins, and specialized joints in the ankle, shoulder, and forelimb for jumping between vertical supports that predominate at this level. The dense vegetation provides insect prey and protection from predators. The reasons for its affinity to the stream edge, secondary growth, and, most particularly, bamboo thickets are that these habitats are where they search for fungal sporocarps, a key food year-round and especially in the dry season.
It is unclear why Amazonian tamarins and marmosets have a propensity to enter and occupy inundated forests, either white-water inundated forest (“várzea”) or black-water inundated forest (igapó). The plant communities of igapó, várzea, and terra firma forests are quite distinct. Confusion arises from poor definition of what is a flooded forest when it is mentioned (seasonally inundated, permanently or occasionally flooded). Different flooding regimes result in very different vegetation. In the case of seasonally inundated forest, whether or not the forest is flooded at the time surveys are conducted is also relevant. Gray’s Red-bellied Tamarins avoid várzea when it is flooded, but they expand their ranges and enter it when it is not. Overall, it would seem that most tamarin and marmoset species do tend to avoid flooded forests and river edge, the exception perhaps being the saddle-back tamarins, which may, with their particular foraging habits low on tree trunks near the ground, make at least seasonal use of the insect migrations during rising waters. A study of habitat preferences of the “Red-cap MustachedTamarin” (S. mystax pileatus) and “Ávila-Pires’ Saddle-back Tamarin” (S. fuscicollis avilapiresi) concluded that terra firma and creek-side forests (suffering occasional flash floods) were the principal habitats, and igapó and palm swamp were marginal habitats. Tamarins are consistently reported to prefer so-called edge habitats, which generally refer to areas of forest disturbance (secondary forest arising from past cultivation, logging, or fallen trees) but include, for example, transitions between terra firma and flooded-forest vegetation.
Habitat preferences of Amazonian marmosets and tamarins are essentially the same. The two genera are mostly allopatric and co-occur in only two regions. Weddell’s Saddle-back Tamarin occurs in the Brazilian state of Rondônia, east of the Rio Madeira, and is sympatric with Rondon’s Marmoset. The Silvery Marmoset in the lowland forest between lower stretches of the rios Xingu and Tocantins overlaps with part of the distribution of the Black-handed Tamarin, which also extends into the higher elevation submontane and montane forests of the Brazilian Shield to the south. There is no physical barrier to prevent the Silvery Marmoset from also ranging onto the Brazilian Shield, but it does not occur there. It has been proposed that its distribution is a recent, perhaps Holocene, expansion into that of the (slightly larger) Black-handed Tamarin; it is possible that the two species are only able to coexist in the richer floodplain forest. The Black-handed Tamarin has the competitive advantage in the predictably less productive forests on the poorer soils of the Brazilian Shield to the south. Some tamarins occur in submontane and montane Andean forests to elevations of about 1200–1400 m, notably the Andean Saddle-back Tamarin (Saguinus leucogenys) and “Graells’ Black-mantled Tamarin” (S. nigricollis graellsi).
Some Amazonian marmosets occupy forest patches in Amazonian-type, sandy-soil savannas in the Tapajós and Madeira basins (for example, the Rio Aripuanã Marmoset, Mico intermedius, and the Silvery Marmoset), and the Midas Tamarin (Saguinus midas) occurs in the Rupununi and Sipaliwini savannas of the Guiana Shield. For some reason, the Black-handed Tamarin does not occur in the gallery forests of the savanna in the eastern part of the Island of Marajó. It does occur on the forested western part of the island, but only tufted capuchins (Sapajus), Red-handed Howler Monkeys (Alouatta belzebul), and Collins’ Squirrel Monkeys (Saimiri collinsi) occur in savannas to the east. Reasons for the absence of the Black-handed Tamarin in the east may due to a lack of key food resources and perhaps competition with squirrel monkeys and capuchins. One of the Amazonian Marmosets, the Black-tailed Marmoset (Mico melanurus), ranges south from the forest of the Mato Grosso into the gallery forests and forest patches of the Pantanal of the Paraguay River and into the Chaco regions of Bolivia and extreme northern Paraguay. They occur in relatively tall subhumid forests in the far east of the Chaco and in tall forests with dense undergrowth along ephemeral waterways (“cauces”).
The Atlantic forest marmosets occur in lowland forest (Geoffroy’s Tufted-ear Marmoset, Callithrix geoffroyi, and Wied’s Black-tufted-ear Marmoset) and upland or montane forest at elevations of 400–500 m to as high as 1200 m (Buffy-tufted-ear and Buffy-headed marmosets). The lowland species occur in evergreen coastal forest with rainfall exceeding 2000 mm and in drier, semi-deciduous forest inland and along some parts of the coast. The upland species occur in highly seasonal forests where fruits are scarce for many months of the year. At these times, they increase their consumption of gums and nectar (and in some cases fungi) and their time foraging for animal prey. The Common Marmoset in north-eastern Brazil occurs in the coastal humid and semi-deciduous (mesophytic) forests to the west, but it also ranges inland along gallery forest and into the highly seasonal dry Caatinga scrub forest. Its occupation of these forests is made possible by its tree-gouging and gum-feeding specialization, but population densities tend to be very low in the driest environments. The Black-tufted-ear Marmoset occurs in seasonal semi-deciduous Atlantic forest and dense Cerrado woodland (“cerradão”), gallery forest, and Mauritia palm swamp (“veredas”) in the Cerrado (tropical savanna) region of central Brazil. Like the Common Marmoset, its tree-gouging and gum-feeding proclivities allow it to occupy highly seasonal forests and woodland characterized by long periods of fruit scarcity. Both these species are highly adaptable, and introduced populations have become established in numerous areas outside their natural distribution, even as far south as the state of Santa Catarina in Brazil and in urban parks in Buenos Aires, Argentina. Atlantic forest marmosets and lion tamarins are largely allopatric, but the Golden-headed Lion Tamarin and Wied’s Black-tufted-ear Marmoset have entirely overlapping distributions in the south of the state of Bahia in Brazil, and the introduced Common Marmoset and the Black-tufted-ear Marmoset now occur in a large part of the remaining forests where the Golden Lion Tamarin still survives in the state of Rio de Janeiro.
All field studies of marmosets, tamarins, and Goeldi’s Monkey have documented their association with the dense vegetation typical of secondary growth, successional forest, and edge habitat. Tracts of tall, late successional and climax forest with sparse, open understories are evidently unfavorable.There are a number of reasons for this. Callitrichids are small and as such vulnerable to a wide array of predators, and the dense vegetation is undoubtedly vital as a refuge and for providing substrates to travel low in the forest without having to go to the ground. The fruiting patterns and clumped distributions of pioneer trees in these successional habitats are also favorable.Colonizing bushes and trees typically produce abundant small succulent fruits over prolonged fruiting seasons. Small succulent berries and drupes available for extended periods in a restricted area are perfect for small marmosets and tamarins, but not for larger primates. In climax forest, trees are more widely dispersed, their fruits tend to be larger, and fruiting occurs irregularly. Dense vegetation also provides the appropriate environment and substrates for foraging on animal prey. The mosaic of successional habitats constantly colonized by these monkeys is highly dynamic; patches of secondary growth arise from tree falls, and new growth is constantly available from primary succession resulting from large-scale natural forest disturbance caused by lateral erosion and channel changes in meandering rivers. Plant communities vary depending on the flooding regime, but Moraceae, Cecropiaceae (Urticaceae), Annonaceae, and Fabaceae (Leguminosae) are important families contributing pioneer species, and all four are of significance in providing fruits and gums to callitrichid diets. Meandering rivers are predominant in the upper Amazon, receiving heavy silt loads from the Andes, and about 27% of the region is characterized by recent erosion and deposition and about 12% is currently in different stages of succession due these processes. Differences in the fluvial dynamics of black-water and white-water rivers also affect abundance of marmosets and tamarins. Rivers flowing off the Brazilian and Guiana shields are old, low in sediment, and do not meander to the same extent as those in the upper Amazon. It is possible that the occurrence of up to four sympatric callitrichids in the primate communities of the upper Amazon, in contrast with just one species (two in some few areas) in the middle and lower Amazon Basin, is related to the high habitat (plant) diversity caused by the instability of the upper Amazon forests resulting from river-channel erosion.
Forests in certain parts of the Amazon Basin typically have larger trees than in other parts, and tree falls may be more frequent in some areas than other areas, depending on soil type and topography (drainage, exposure to wind). Size, abundance, and spatial patterns of tree falls that open the canopy and encourage succession affect plant composition of the forest and availability of suitable habitat mosaics for colonists such as marmosets and tamarins. Clearings made by humans—cutting down trees, creating paths, and cultivating small gardens—now constitute important habitats for many of these primates. These anthropogenic habitats may influence distributional patterns and abundance of these primates in natural forests, which result from subtle but major forces determining plant composition, forest architecture, and mosaic patterns of succession. It is possible that the ranges of the Black-handed Tamarin and the Silvery Marmoset (latter restricted to the alluvial plain of the Rio Amazonas, and the former extending onto the Brazilian Shield) are determined by distinct patterns of successional forests and plant communities. Likewise, ranges of the Pied Tamarin (Saguinus bicolor) and Martins’ Bare-faced Tamarin (Saguinus martinsi) are restricted to the alluvial plain of the Amazon, possibly a result of their former isolation, and a major change in the river course in the past. The Midas Tamarin occurring on the Guiana Shield is now entering the range of the Pied Tamarin in the alluvial plain of the Rio Amazonas and displacing it; forest destruction and disturbance by humans are considered to be the causes. Martins’ Bare-faced Tamarin may be suffering the same fate with forest destruction in the lower reaches of the Rio Trombetas.
The four lion tamarins occur in the Atlantic forest of Brazil. The Golden Lion Tamarin, the Black-faced Lion Tamarin (Leontopithecus caissara), and the Golden-headed Lion Tamarin occur in the lowland moist forest of the coastal regions east of the Serra do Mar. The Golden-headed Lion Tamarin also occupies more seasonal semi-deciduous (mesophytic) forest further inland. The Golden-headed and the Black-faced lion tamarins also inhabit coastal, sandy-soil forests, regionally known as “floresta de restinga,” as did the Golden Lion Tamarin in the past. The range of the Golden-headed Lion Tamarin covers the cacao-growing region of southern Bahia, and it has been found in older plantations that use trees of the original forest cover and cultivated fruit trees—an agroforestry system regionally called “cabruca.” Two important elements of the habitats preferred by the coastal lion tamarins are large epiphytic tank bromeliads (where they forage for animal prey and eat the fleshy, pineapple-like, multiple fruits) and tree holes that they prefer as sleeping sites. These habitat aspects and the relatively large size of lion tamarins and their tendency to forage for animal prey in the canopy layers of the forest rather than the understory indicate that they evolved to exploit tall mature (lowland) forests. If, however, sufficient prey foraging sites (particularly bromeliad epiphytes) and fruit or gum sources exist, lion tamarins can use secondary and degraded forest for the same reasons that these habitats are favoredby marmosets. Golden-headed Lion Tamarins are able to survive in degraded and successional forests, and groups have even been found living exclusively in cabruca when they are able to rely on a minimum number of trees providing fruits throughout the year, such as jackfruit, Artocarpus heterophyllus, and figs, Ficus gomelleira (both Moraceae). All forests where Golden Lion Tamarins now survive are disturbed, logged, and secondary in various stages of succession. The Black-faced Lion Tamarin, the southernmost of the callitrichids, is the only one of the four species that can still be found in large tracts of tall, relatively pristine, mature lowland forest. All lion tamarins favor swampy and creek-side forest, not only to forage for prey (more humid environments where insect communities can thrive) but also because of the availability of Symphonia globulifera (Clusiaceae) that provides nectar when fruit are scarce. Within their home ranges, they use swampy and seasonally (briefly) inundated areas intensively and also secondary forest patches more than would be expected by chance.
Lion tamarins largely occur in lowland forests. For some reason not yet understood, Black-faced Lion Tamarins do not occupy submontane forest available to them at elevations above 40 m. The Golden Lion Tamarin, otherwise occupying the coastal lowland forest, range up eastern slopes of the Serra do Mar to about 380 m above sea level. Nevertheless, groups have been seen at elevations of 530 m and 550 m, and there is some speculation that lion tamarins have been forced up mountain slopes because of destruction and fragmentation of lowland forests and that their survival at these higher elevations may depend on their use of cultivated fruits (bananas) and secondary vegetation from human settlements and slash-and-burn plots. Like the Golden Lion Tamarin, the Golden-headed Lion Tamarin was thought to occur only at elevations below about 300 m, but some groups have now been seen at elevations of 500–750 m. The Black Lion Tamarin (Leontopithecus chrysopygus) occurs inland in semi-deciduous and riparian forests in the state of São Paulo and naturally occupies forest at higher elevations, with a more accentuated seasonality in rainfall and fruit availability than is typical of the coastal forests. There is a record of one sighting at 937 m above sea level at Pilar do Sul in the Serra da Paranapiacaba in the south-eastern part of its range.
General Habits
All marmosets and tamarins can be classified as quadrupedal runners and jumpers, but they are unique among New World primates in their predominance of vertical-clinging postures, made possible by claw-like nails that allow them to grasp the sides of large-diameter tree trunks. Vertical clinging and leaping are forms of locomotion that are most accentuated in understory dwellers where tree trunks, lianas, and saplings predominate: the Pygmy Marmoset, saddle-back tamarins, the Black-mantled Tamarin (Saguinus nigricollis), Goeldi’s Monkey, and, undoubtedly, the little-known Black-crowned Dwarf Marmoset. Goeldi’s Monkey generally travels at heights below 5 m above the ground and rarely goes above 10 m. It is the strongest leaper, and more than one-half of its leaps are between vertical supports; in contrast, tamarins leap trunk-to-trunk 8–20% of the time. In Callimico, vertical clinging and leaping account for 45% of five locomotory behavioral categories compared to 22% for saddle-back tamarins and 3% for middle-canopy-dwelling Red-bellied Tamarins (Saguinus labiatus).Callimico has relatively long hindlimbs (the lowest intermembral index of any species of the family) along with anatomical modifications of the ankles (shared with the sakis, Pithecia) that increase stability and represent adaptations for leaping and vertical clinging. When leaping, they land hands-first and can jump further than marmosets or tamarins—up to 2 m (ten times their body length) and with little or no loss of height in doing so. The Common Marmoset by comparison can leap up to 1·7 m but loses height. Callimico is also unique among callitrichids in its use of so-called “hindlimb-dominated bounding”—hopping like a rabbit.
Marmosets and tamarins occupy forests or forested areas (for example, savanna forest or gallery forest) that have variably seasonal rainfall and temperatures at the higher latitudes and elevations. Rainfall patterns determine seasonal changes of fruiting, flowering, leaf growth and, in the drier climates, leaf fall. These seasonal changes of the plant communities affect not only the availability of plant foods to these primates but also seasonal and overall insect prey abundance. Although broadly classified as insectivore-frugivores, plant exudates are eaten by all species of callitrichids and are an important element of the diet of many. The exudates are mostly gum and nectar, but there are also some cases where latex, resin, and sap are consumed. For all species, these exudates are, it would seem, a fallback during seasonal fruit shortages, but for some species, especially marmosets that gouge holes in tree trunks, branches, and vines of numerous plant species to cause the flow of gums, these exudates are eaten year-round. Tamarins and lion tamarins are able to eat gums only when they are readily available; for example, when they are exuded spontaneously in some fruits, the seed pods of some of the large Parkia (Fabaceae) trees, or due to breakage, wind damage, or wood-boring insects. The ability to rely on gums year-round has profound consequences for the marmosets. Gums are a fundamental food resource for the Pygmy Marmoset and probably the Black-crowned Dwarf Marmoset . Both are too small to occupy home ranges large enough to contain trees providing fruit year-round, and they have well-developed behavioraland morphological adaptations for tree-gouging and gum-feeding. They are best classified as insectivore-exudativores (they are also referred to as gummivores, emphasizing the gum-eating aspect of their diet). It is evident that the larger marmosets will always eat fruits when they can, but their gum-feeding specializations mean that they can occupy highly seasonal forests where fruits can be generally scarce or lacking for prolonged periods.
Exudate consumption is not equal among species of callitrichids. Common and Black-tufted-ear marmosets are the most specialized and highly exudativorous, and they are able to occupy the most unfavorableand seasonable habitats. Wied’s Black-tufted-ear and Geoffroy’s Tufted-ear marmosets are generally less extreme in their tree-gouging and gum-feeding, living in humid coastal or semi-deciduous and less seasonal forests. The Buffy-tufted-ear Marmoset and the Buffy-headed Marmoset (Callithrix flaviceps) form a third group that occupy seasonal, high-elevation forests where exudates are a fundamental component of their diet, but they do little gouging to obtain them, exploiting (trap-lining) readily available gum resulting from wind damage or wood-boring insects. In certain areas, they also eat fungi when fruits are scarce. The extent of tree-gouging to obtain gum among Amazonian marmosets (Mico) is variable, but it is still a fall back resource when fruits are scarce. The lower incisors of Amazonian marmosets are intermediate in size and shape between Common Marmosets and tamarins. Amazonian marmosets and the Buffy-headed and Buffy-tufted-ear marmosets are the least specialized in their dental morphology, and Black-tufted-ear and Common marmosets are the most specialized for gouging. Tamarins and lion tamarins eat readily available gums or nectar at times of fruit shortage. Goeldi’s Monkeyeats gums when it can at times of fruit shortage, but it also specializeson scattered and scarce fungi as a year-round food, which results in relatively large home ranges.
Home ranges of callitrichids vary considerably from 0·5 ha (Cebuella) up to 300 ha (Black Lion and Black-faced Lion tamarins). Home-range size is associated, in part, with dietary specializations and abundance, dispersion, and seasonality of food resources. The highly exudativorous marmosets (Pygmy, Black-crowned Dwarf, Common, and Black-tufted-ear marmosets) are able to occupy small home ranges of less than 10 ha when depending on a single source or a few very clumped sources of gum that they can exploit year-round. Home-range size in these species is probably determined more by availability and renewal of animal prey. Other species of marmosets, while still having a considerable exudate component of the diet, have home ranges of 10–40 ha. Tamarin social groups generally occupy home ranges of 40 ha or more, being opportunistic in their consumption of gums and often eating nectar at times of fruit shortage. Areas occupied by groups of Goeldi’s Monkey range from 90 ha to 150 ha, likely due to their dependence on diffuse, small patches of fungi at times of fruit shortage. The lion tamarins use remarkably large home ranges, as large as 300 ha, but when secondary forests provide ample fruits, preferred prey-foraging sites are abundant, and little competition occurs with other primates, their home ranges can be as small as 40 ha. Being site-specific foragers in the forest canopy and evidently adapted to mature forests where fruit sources are widely dispersed and possibly fruiting irregularly, they require very large areas to overcome the great degree of spatial unpredictability than is the case in secondary growth and forests in the early stages of succession. Prey renewal rates at foraging sites may also be a key factor. Understanding variation in home range demands an understanding of the spatial and temporal patterns of food availability.
Where they are sympatric (east of the Río Ucayali, south of the Rio Amazonas, east to the Rio Madeira), saddle-back tamarins (nominate race of Spix’s Saddle-back Tamarin, Ávila-Pires’ Saddle-back Tamarin, Geoffroy’s Saddle-back Tamarin, Saguinus nigrifrons, and Weddell’s Saddle-back Tamarin, Saguinus weddelli) tend to form “mixed-species groups” with the “mustached tamarins”(Mustached Tamarin, Saguinus mystax, Red-bellied, or Emperor tamarins). A saddle-back tamarin group and one of the mustachedtamarin species join up and travel together during the day. The smaller (342–411 g) saddle-back tamarins travel low in the forest, from the ground up to 10 m, and the larger mustachedspecies (for example, adult Mustached Tamarins 488–576 g) travel above them in the lower and middle canopy, above 10 m. The groups sleep in separate locations from 20 m to 100 m apart, and in the morning, they search each other out, often calling. They occupy a home range together and defend it against neighboringconspecific groups. Mustached tamarinstend to move faster than saddle-back tamarins, which follow.These associations suggest that the mixed species must be very similar in terms of their habits and needs but different enough to avoid competition. There must be advantages to traveling together that override any possible disadvantages from competition. The general findings are that the fruit proportion of their diet overlaps considerably, notably in the exploitation of larger-canopied trees with abundant small fruits, but there is no evidence of competition (no displacement or dispute). The infrequent interactions between individuals of each species are most often over less abundant food in small-canopied trees, and larger mustached tamarinsdisplace smaller saddle-back tamarins. The two species diverge most in their selection of prey, exploiting different prey and using different foraging methods at different heights in the forest. In their different foraging modes—visual-searching foraging and manipulative foraging—saddle-back tamarins tend to take larger insects, which are more often brown or gray(camouflaged in dark and woody places) rather than green, and mustached tamarinstake smaller, mostly (almost exclusively) green prey hiding under leaves and branches in the canopy above them. Saddle-back tamarins sometimes capture insects that have been flushed by mustached tamarinsabove them and have fallen to the ground. Saddle-back tamarins spend less time foraging for prey than mustached tamarins,indicating that they may be more efficient in satisfying their daily needs. The time that saddle-back tamarins spend in association varies from day-to-day, but it also depends on which species of mustachedtamarin is involved; saddle-back tamarins are more avid in their association with the Emperor Tamarin than with the Red-bellied Tamarin, and relatively little time is spent in association with Emperor Tamarins. The degree of association between the different species pairs is correlated with the degree of segregation in their vertical use of the forest—the Mustached Tamarin uses higher levels, the Red-bellied Tamarinuses slightly lower levels, and the Emperor Tamarinspends more time in the understory than the other mustachedspecies, overlapping somewhat with the saddle-back tamarins. These differences may reflect increasing degrees of overlap in where in the canopy (heights) and how prey is searched for, hence increasing inconvenience for saddle-back tamarins.
A comparative study of habitat use by the Weddell’s Saddle-back Tamarin showed that they use small (less than 5 cm in diameter), medium, and large branches (more than 10 cm in diameter) in roughly equal proportions, whereas Red-bellied and Mustached tamarins use small supports more and larger supports less. Saddle-back tamarins use horizontal supports much less and vertical supports much more than do mustached tamarins,and they spend much more time on tree trunks and much less time on branches than do mustached tamarins.When jumping, saddle-back tamarins go from a branch to another branch much less and from a branch to a trunk, or jump between trunks, more than mustached tamarins,which mostly jump from branch to branch. Saddle-back tamarins forge for animal prey at a mean height above the ground of 6·1 m, and11·2 m when foraging for fruits. In contrast, mustached tamarinsforage for insects at a mean of 9·4 m above the ground and for fruits at 16·7 m. Saddle-back tamarins will spend 44·7% of their time foraging on bark, 39·4% on leaves, 13·2% in crevices and holes, and 2·6% in epiphytes. In contrast, the Red-bellied Tamarinforages on leaves 87·1% of the time and the remainder of the time on bark. Emperor Tamarins prey on insects at a mean height of 9·4 m above the ground and forage for fruits at 16·7 m, but they spend 90% of their time foraging on leaves. These measurements clearly define structural and vertical differences in the habitats used by these species, which, along with differences in foraging techniques and sites, result in clear differences in the animal prey they eat.
Although mixed-species groups travel together during the day, they separate in the late afternoon to go to different sleeping sites. Mustached tamarinsuse sleeping sites at higher levels in the forest than saddle-back tamarins, but they are generally close, and in the morning, they reestablish contact using loud calls. If they lose contact during the day (for example, as happens sometimes following intergroup interactions), they give long calls to reestablish contact—one group does not just tag along with the other, they actively seek to stay with each other. Mustached tamarinsgenerally take the lead when traveling, and they are usually the first to enter fruiting trees. The benefits of mixed-species groups probably include enhanced feeding efficiency and predator defenseand vigilance. Traveling in a larger group means that there are more eyes to detect predators. When a predator or likely predator is seen, they give alarm calls, and each species responds to the alarm call of the other. The same result could be achieved if each species formed in larger groups, but there are evidently social and reproductive issues with regard to doing this, and group sizes of mustached tamarins are generally smaller than those of marmosets, for example, which often breed twice rather than once-a-year, typical of Saguinus. Another aspect is the dilution effect; in a larger group any one individual is less likely to be caught, assuming all are equally careful and attentive. Whether each of the groups experiences less predation in association with the other than when traveling alone is difficult to test, but it is possible to examine differences in vigilance—the rate at which a tamarin stops other activities to scan its surroundings. This is not a perfect correlation, of course, because a tamarin can be looking around for many reasons, not just for predators, but it is presumed that each individual would scan less (and have more time to do other things) in a larger group than in a smaller group. This seems to be the case in mixed-species groups of Red-bellied and Spix’s Saddle-back tamarins; the overall vigilance of (larger) mixed-species groups was higher compared with single-species groups, but despite this, there were fewer times when no individual was scanning. Presumably, vertical segregation of the two species means that their vigilance covers a larger volume of the forest than would be the case for each species on their own. Saddle-back tamarins in the understory look down more and are more liable to detect terrestrial and scansorial predators, and mustachedtamarins scan more in the middle and lower canopy where the aerial predators are a greater threat. Mustached tamarinscan be more vigilant (higher scan rates) than saddle-back tamarins, which might be related to the fact that hawks and eagles are more common predators of callitrichids than terrestrial predators (although this may be because human observers frighten away terrestrial predators more than they do aerial predators). Saddle-back tamarins scan looking up more often when they are in single-species groups than in mixed-species groups.
Increased foraging efficiency also may promote formation of mixed-species groups. There is evidence that saddle-back tamarins benefit from catching grasshoppers and other insects that fall to the forest floor after being flushed by foraging mustached tamarinsabove them. Sharing the same home range may enhance each species’ knowledge of plant food sources at different heights in the forest. Mustached tamarinsfind more large food patches in the upper strata of the forest than saddle-back tamarins (a benefit to saddle-back tamarins), and saddle-back tamarins find more smaller food patches than mustached tamarinsin the understory (mustached tamarinsbenefit because, being larger, they displace the saddle-back tamarins)—a sort of mutual parasitism or quid pro quo. Another possible benefit is that each species gains monitoring food sources used by both; by traveling together, they are able to coordinate the harvest of food resources from the different parts of their home range.
Goeldi’s Monkeysalso travel with mixed-species groups of mustachedand saddle-back tamarins (forming polyspecific groups), moving and foraging below the saddle-back tamarins. Goeldi’s Monkeyhave much larger home ranges (100–150 ha) than tamarins, so they may associate with up to five different tamarins groups. Groups of Goeldi’s Monkeygroups travel with tamarins for about 50% of their time but leave tamarins behind when they enter bamboo forest and stream edge to look for fungi. Monthly association rates between Goeldi’s Monkeys and tamarinsvary with the dietary compatibility and range from 89% of the time in a wet season month with abundant fruits to 13% in the dry season, when Goeldi’s Monkeysfeed more on fungi and tamarins on nectar and gums. Associations of Goeldi’s Monkeyand tamarins likely provide benefits from shared knowledge of the location of fruit trees and increased vigilance for predators in larger groups. Weddell’s Saddle-back Tamarin is sympatric with Rondon’s Marmoset in some localities east of the upper Rio Madeira. They too form rather loose mixed-species groups; a study recorded groups close to each other on most days, and they would spend all day together when sharing abundant foods such as Parkia gum or Symphonia flowers. Saddle-back tamarins exploit the gum sources maintained by the gouging of marmosets. The Golden-headed Lion Tamarin is sympatric with Wield’s Black-tufted-ear Marmosets, but they do not form mixed-species groups very often. In one study, they did in 36 of 130 occasions, ranging in duration from five minutes to over two hours and averaging 80 minutes, and perhaps largely a coincidence of food availability and common travel routes. Their diets overlap with some abundant fruits and flowers, but lion tamarins have much larger home ranges than marmosets and their rate of travel and their foraging locations and techniques for obtaining animal prey are distinct enough to minimize formation of mixed groups.
Because of their relatively large groups, considerable degree of sociality, coordination and cooperation in predator defense, breeding, movements and foraging, and territorial behavior, callitrichids show complex and varied communication, interacting with members of their own groups and their neighbors.They use visual patterns (to some degree facial expressions but also body postures including tail positions and pilo-erection), vocalizations (contact calls, warning calls, mobbing calls, food calls, and agonistic utterances of fear and aggression), tactile patterns (biting, huddling, grooming, mounting), and olfactory patterns (scent marking). Elements of all these manners of communication are used in combination and sequentially, and they result in an extraordinarily rich repertoire of signals and messages, albeit still poorly understood relative to context and motivation.
Facial expressions are rather limited (perhaps in part due to our inability to perceive the subtleties). Goeldi’s Monkey, the Pygmy Marmoset, and the rest of the marmosets frown. The Common Marmoset can show a “slit-stare” (staring, partially closing its eyelids) and can also raise and lower its fan-like ear tufts. Frowning is aggressive, and frowning with ear tufts erect is more so. A partially open mouth with a slit-stare indicates alarm, and ear tufts flattened with a slit-stare are submissive. The Pygmy Marmoset has a distinct scared-face and flattens its fur, pulls back its eyebrows and ears, and flattens itself against a branch when submissive. Bared-teeth grins, common to so many primates, indicate fear and submission, are graded in the extent and duration of the grin (combined with ear tufts flattened, slit-staring, and “geckering” calls, and screams when extreme), and can be accompanied by cringing. In marmosets, lip-smacking and rhythmic “slow tongue in/out” are seen infrequently when grooming, and sometimes faster tongue movements with lip-smacking are seen during sexual solicitation. Tongue-flicking or “tonguing,” as it is called, is also associated with mating in the Pygmy Marmoset, tamarins, and lion tamarins. Very rapid tongue in/out associated with aggressive vocalizationshas been seen in the Silvery and Black-tailed marmosets, the Emperor Tamarin, and the Pied Tamarin.
The tail of callitrichids is coiled over the shoulder and along the back when resting or sleeping. They often scratch their tails, raising themup between their legs, holding themwith one hand and scratching themwith the other. This is done briefly in a relaxed peaceful way at intervals throughout the day, but during social commotion, especially encounters between groups, it is frantic and frequent, evidently signifying excitement or even stress. In these cases, it is referred to as displacement scratching, and the back and thighs also are scratched. Tail coiling is evidently a communicatory device for at least some species. Either while hanging or held below and behind the body, tail coiling is seen during copulation in marmosets and as a pre-copulatory display in tamarins. Tail coiling as a visual display has not been noted for the Pygmy Marmoset or lion tamarins. Very striking tail-thrashing, wagging or “tail-snake,” is seen rarely, but it is associated with stressful situations in the Pygmy Marmoset, marmosets, and lion tamarins. In the Rio Aripuanã Marmoset, at least, it also may express a degree of frustration, being seen on a few occasions in individuals waiting their turn to feed on gum, where a small tree trunk and relatively few gouge holes resulted in a clear, hierarchical situation where dominant group members feed first.
Piloerection patterns are striking and ritualized, most frequently expressed in the “arch-bristle walk” (fur erect, stiff legs, back-arched, and a slightly awkward walk) and seen variably in encounters between groups, in agonistic situations within the group, and when a male is following a breeding female in what is believed to be “mate guarding.” A common aggressive signal in Pygmy Marmosets and other marmosets is called “tail-raise present,” seen especially during encounters between groups. With its fur raised to make it look fluffier and bigger, a marmoset will turn round in a deliberate way, look back over its shoulder, and raises its tail to present its white genitals. This is sometimes done by several members of a group simultaneously to an opposing group that is behaving in similar fashion on a branch some few metersaway—a sort of “standoff.” Males pulse their testicles, pulling them in and pushing them out. Genital or rump displays with the tail raised are also seen in mating contexts in Pygmy Marmosets, marmosets, and tamarins.
Vocalizationsare high-pitched and birdlike. They are difficult to describe, and in the social context among group members, the chatters, grunts, coughs, whistles, squeaks, trills, squawks, “eks,” “tsacks,” cackles, chirps, and peeps, to name a few, are generally difficult to understand relative to their function and motivation. A broad sweep on the context accompanying signals and the age or perceived rank of the emitter of these noises can only give a general idea of submission, dominance, fear, aggression (agonistic), discomfort, surprise, and so on. It is possible to categorize them in this way, but a clear understanding of meaning can only be ascertained by close observation and sophisticated experimentation in captivity. Contact calls, often described as long calls, are used to maintain contact between group members as they travel through their home range during the day. They are distinct and identifiable for each species. There is undoubtedly much more information in these calls, however, than just “I am here.” An investigation of the long calls of the Cotton-top Tamarin, for example, showed that they are not merely species-specific but group-specific, as shown by isolating members of different groups in captivity within hearing distance of all and seeing which groups and individuals tend to reply to the isolated individual’s calls. Every contact call probably is identifiable to sex or individual and varies in other aspects of information transmitted, such as emotion and situation. Food calls that alert group members to a find of fruit or gum have been identified in the Red-bellied Tamarin,. Contact calls vary from rather low chirps when the group is close together to the drawn out and frequently repeated long, or “phee,” calls when the group is spread out.
Mobbing occurs when the whole group concentrates around something or some other animal they perceive as a threat. Their movements during mobbing are agitated, with jerky head-movements, looking away and then looking back to the source of their disturbance, often head-cocking, and emitting a staccato of calls that are described as “tsiks,” clicks, and tonal squeak-clicks in the Pygmy Marmoset, “tsacks” in marmosets, squeaks, chirps and slicing screams in Cotton-top Tamarins, trills with warble mews and staccato mews in Illiger’s Saddle-back Tamarins (Saguinus illigeri), and clucks (along with trills) in lion tamarins. Warning calls alerting to aerial predators tend to be loud, short, and very high-pitched single calls, sometimes repeated instantly by other group members, followed by a rapid flight to the understory and cover where they freeze and remain silent. Agonistic calls used in different situations with all sorts and degrees of arousal are generally atonal and rasping squawks, coughs and screams. Calls associated with food sharing by adults to infants and juveniles have been perceived in lion tamarins: an individual as a giver emits a low “wah-wah” call, causing a nearby infant, perhaps already begging for a morsel, to come running and snatch the item. The infant’s snatching, while emitting begging calls, makes it difficult to discern if the interaction is one of stealing, stealing with permission, or an actual offering—the wah-wah call suggests an offering.
Tactile patterns of communication include play wrestling, huddling, allogrooming, and, rarely in agonistic situations, butting or shoving, cuffing, and biting. Perhaps the most extraordinary and intriguing forms of communication among callitrichids are olfactory. All callitrichids have epidermal scent glands specialized for communication. There are three glandular fields: anogenital, suprapubic, and sternal. Female Pygmy Marmosets, marmosets, and tamarins in estrus rub their anogenital region on males and vice versa (allomarking), probably playing a role in advertising female reproductive condition and soliciting copulation and, for males, allomarking females and mate guarding. In a captive experiment with the Cotton-top Tamarin, the scent of a breeding female was placed daily in the cages of eight male–female pairs. During the periovulatory period (three days around the urinary luteinizing hormone peak), females investigated the scent more than males, and males showed increased penile erection rates and mounting. For Geoffroy’s Saddle-back Tamarin, overmarking of a female’s scent marks by a male may be a way of obscuring information on the female’s reproductive status to other group members, and as such, a form of mate guarding. The most frequent use of these scent-gland fields, however, is leaving olfactory messages on branches and tree trunks with stereotypical behaviorsof sit-rubbing (anogenital shuffling forward a little in a sitting posture, often rubbing on a small protrusion on the branch), touching, rubbing, or dragging the suprapubic area along a branch, or doing the same with the sternal region. Lion tamarins sit-rub with their legs dangling on either side of branches as they pull themselves forward. The three glandular areas are not used with equal frequencies and contain different messages, serving different functions. Their use appears to differ between sexes and, seemingly, among different species. They are directed toward group members and certainly perceived by neighboringgroups, and they play roles as such in territorial behavior, probably dominance (hierarchical relations as we see them), and reproductive status . Too little is known about scent marking in most species of callitrichids to be able to generalize, but there have been some studies of this behavior in the Common Marmoset, Geoffroy’s Tamarin, the Cotton-top Tamarin, the Pied Tamarin, and saddle-back tamarins in captive conditions, and Geoffroy’s Saddle-back Tamarin, the Mustached Tamarin, the Buffy-headed Marmoset and the Rio Aripuanã Marmoset in the wild.
Anogenital, suprapubic, and (rarely) sternal marking have been observed in the Rio Aripuanã Marmoset and Wied’s Black-tufted-ear Marmoset in the wild, but only anogenital and, less commonly, sternal marking in the Buffy-headed Marmoset. Suprapubic marking, frequent along arboreal pathways, is possibly a form of territorial marking, not to defend the home range as such but to register and demarcate ownership, allowing for scent matching during encounters between groups. Scent marks are scattered throughout a home range and do not demarcate its boundaries. Marmosets scent-mark more in areas where they spend more time. There is considerable suprapubic marking, and occasionally sternal marking, during intergroup encounters, although not necessarily more than at other times. Every so often, group members come together during the most agitated moments of an intergroup encounter and huddle, groom, and scratch in a perfunctory and excited way, and then will suddenly break off and sometimes, in turn, suprapubic mark a nearby spot (collective marking) and rush off to chase the opposing group. Sometimes members of the neighboringgroup overmark that same spot during the encounter. Some of the most actively used of the suprapubic scent mark spots are gouged by marmosets, probably not to obtain exudate but to increase absorption and permanence of the scent marks. This territorial function (not ruling out other possible functions) of suprapubic marking may mean that it is not seen in captive conditions due to the lack of context. Sternal marking is infrequent in marmosets and tamarins; it appears to have a more intensely aggressive function and is seen sometimes during intergroup encounters. Sternal marking has been seen in Geoffroy’s Saddle-back Tamarin and the Midas Tamarin but not the Cotton-top Tamarin, and its contexts and message remain a mystery.
Anogenital (also referred to as circumgenital) marking is undoubtedly linked to the transmission of information on reproductive status and perhaps hierarchical status, and it quite possibly has a pheromonal role in the physiological inhibition of ovulation of subordinate marmosets and tamarins by a breeding female. Notably, marmosets tend to rub their anogenital glands (often placing a drop of urine too) in the holes they gouge in vines, trunks, and branches to provide gums. Gouge holes are the one place in the forest where all group members frequently place their noses and even lick and eat the scent mark. Anogenital marking in Rio Aripuanã Marmosets is seen infrequently and always in sexual contexts (for example, just after copulation). While gum comprises a major proportion of the diet of Buffy-headed Marmosets, they gouge branches and trunks infrequently. They obtain most of their gum from trap-lining spontaneously exuded Acacia gum at numerous sites. Rather than marking in gouge holes, these marmosets can be seen anogenital marking numerous sites in their home range along branches (often with a visible protuberance that stimulates output of glandular exudates). Infrequent use of gouge holes by the Buffy-headed Marmoset evidently makes them ineffective as scent marking sites.
Food and Feeding
All callitrichids are fruit eaters (frugivores) and small animal predators, eating small arthropods, snails, frogs, lizards, birds’ eggs, and nestlings (insectivores or carnivores). All callitrichids also eat plant exudates, mainly nectar and gums (also rarely latex), which is a defining feature of these primates. Marmosets are specialist gum feeders and have morphological adaptations to gouge tree trunks, branches, and vines to obtain it, ferment it, and digest it. Tamarins, lion tamarins, and Goeldi’s Monkey eat gums opportunistically, but they may still comprise a significant proportion of the diet at certain times of the year when, for example, fruits are scarce. Fungi are eaten by a few species of callitrichids and are a significant component of the diet of Goeldi’s Monkey and some populations of at least two of the Atlantic forest marmosets.
Soft fruits, most often in the form of berries and drupes, are eaten by all callitrichids; many of them are coloredyellow-orange, red or purple. The majority of soft fruits are eaten in middle and subcanopy layers of the forest, 11 m or more above the ground, but some from 20 m up to 30 m in the tallest forests. Although fruits of a large number of plant species are eaten, numerous studies have indicated a general pattern of relatively restricted use of a number of plant species throughout the year. The fruit crops of these species ripen over prolonged periods and only a small number are available at any one time, providing a reliable and prolonged source of fruits. This pattern of fruit availability is appropriate for small primates living in small groups, but fruits are too few, often too small, and too diffuse to be useful food sources for larger primates, particularly those living in larger groups. Although a group of callitrichids may eat fruits of 20 or more different plant species in months when fruit is most available, generally only two or at most three fruit types constitute the majority of the fruit in the diet. During the rainy season in November–February when fruits are abundant, for example, a group of Rio Aripuanã Marmosets ate fruits from 13 to 16 different species each month, but averaged throughout the year, fruits from just three plant species contributed 60–80% to the plant part of the diet. In other dry-season months, the relative lack of fruits resulted in marmosets eating more gums and nectar, but even so, in all but April, fruits and exudates from just three plant species accounted for 50–80% of the plant diet. In April, a time of severe fruit shortage, six of 26 species accounted for 50% of the diet, including sources of exudates, flowers, and nectar. Just a few species with prolonged fruiting and piecemeal ripening basically supplied the large majority of plant food items eaten by marmosets throughout the year: Pourouma palmata and P. acuminata (Cecropiaceae), Pseudolmedia laevigata (Moraceae), two species of Inga (Fabaceae; one of them Inga thibaudiana), Pouteria (Sapotaceae), and Cecropia sciadophylla (Cecropiaceae), along with the nectar of Symphonia globulifera (Clusiaceae [Guttiferae]). All of them were abundant in the secondary forest patches preferred by marmosets. A similar pattern was found for mixed-species groups of Weddell’s Saddle-back Tamarin and the Emperor Tamarin at Cocha Cashu, Manu National Park and Biosphere Reserve in Peru. There, fruits of the semi-lianous shrub Celtis iguanea (Ulmaceae) accounted for up to 90% of the monthly diet over three months; Guatteria (Annonaceae) fruits comprised 61% of the diet in November when many other trees are fruiting. The grape-like fruits of Pourouma cecropiifolia (Cecropiacae) were a key resource during the dry-season months of August–November. For all of these species, except Guatteria, marmosets and tamarins swallow the seeds and act as seed dispersers by excreting them intact. For plant species that figure so prominently in the diet, the role of marmosets and tamarins as seed dispersers is probably of considerable importance in the dynamics of plant communities, including secondary succession after disturbance.
Seed swallowing and seed dispersal have been investigated in a number of species, including tamarins (Geoffroy’s, Black-handed, Mustached, Spix’s Saddle-back, and Geoffroy’s Saddle-back tamarins) and lion tamarins (Golden and Black lion tamarins). Studies of the feeding ecology of the Mustached and Geoffroy’s Saddle-back tamarins at the Rio Blanco Research Station on the Río Tahuayo, Peru, investigated their role as seed dispersers. In a 43-day study of mixed-species groups of the two species by P. Garber, tamarins dispersed (ingesting and defecatingintact) seeds of 17 species. Seeds swallowed by tamarins in this study were not just tiny, mixed in with pulp (the case, for example, with Cecropia fruits), but large and sometimes heavy (average 0·68 g), ranging from 0·7 cm to a little over 2 cm in length. Seed dispersal of Asplundia peruviana (Cyclanthaceae), a hemi-epiphyte that begins its life as an epiphyte on the trunks of small trees but later grows roots to the ground, is curious; its seeds need to be deposited in appropriate sites for germination. The ingestion of its fruits and seeds by Geoffroy’s Saddle-back Tamarinevidently causes diarrhea, resulting in the tamarins defecatingon the trunk where the seeds are able to germinate. Compared with many other fruit-eating primates, seeds swallowed and dispersed by tamarins are extremely large. Fruits are often single, large seeds surrounded by a thin gelatinous and adhesive pulp, or with numerous large seeds surrounded by a fibrous pulp or an aril. Seeds passed through the digestive tract in 1–5 hours, and mostly before noon following early morning bouts of eating fruits. Dispersal distances (from tree to defecationsite) ranged from 34 m to over 500 m. For about 50% of the “dispersal events,” seeds were dropped more than 200 m from their parent tree.
Further studies at the Rio Blanco Research Stationby C.Knogge and colleagues showed that their roles as seed dispersers were even more extensive than was first thought. Seeds (82,405 of them) were found in more than 90% of more than 2000 fecalsamples obtained from the two tamarin species. The number of seeds per sample ranged from one to more than 4800. The seeds were from 88 plant species of 29 families; 67 of the 130 plant species eaten by the Mustached Tamarin and 81 of the 124 plant species eaten by Geoffroy’s Saddle-back Tamarin. Predominant in terms of the number of dispersal events (presence of one or more seeds in a fecalpellet) were the seeds of Anomospermum grandifolium (Menispermaceae) and Parkia panurensis (Fabaceae); in the latter species, seeds were ingested with the gum exuded by the seed pod. Seed length in this study varied from 0·06 cm to 2·35 cm, and seed weight ranged from 0·00004 g to 2 g.
Although numbers of seeds dispersed were heavily biased toward fruits that were most prominent in diets of the Mustached Tamarin and Geoffroy’s Saddle-back Tamarin , the importance of a dispersal event for a particular plant species does not depend on the total number of seeds dispersed but on the proportion of its total fruit crop dispersed. For this reason, some of the few seeds of a particular species that are dispersed by Geoffroy’s Saddle-back Tamarin, for example, may be of considerable importance to the small fruit crop of a small-canopied understory tree. Even when fruit crops are large, tamarins play a major role in the dispersal of the seeds. For the giant emergent tree, P. panurensis, for example, it has been calculated that about two-thirds of the seed crops of three trees were dispersed by tamarins. Fecesof tamarins often contain a single seed thinly smeared with fecalmaterial. The number of seeds in a fecalpellet of any particular species averages 1·2, with a range of one to more than ten seeds. Despite their small size (a mean of 1·4 g), however, tamarin fecesstill, within minutes, attract dung beetles, which bury the fecesand any seeds within them a few centimetresbelow the leaf litter and soil surface, removing them from easy detection by seed predators. Seeds in tamarin fecessuffer lower predation rates from insects or rodents, for example, than those in the more voluminous fecesof larger primates such as spider and howler monkeys. The low seed density in tamarin feces also reduces competition among sprouting seedlings.
Why do marmosets and tamarins swallow these relatively large seeds when they obtain no nutritional benefit from doing so? The seeds fill up the intestine and have to be excreted without delay to allow marmosets and tamarins to continue foraging and feeding. The energy content and nutritional value of the fleshy or gelatinous mesocarps of drupes and berries and fleshy arils, coating the seeds, for example, of Inga (Fabaceae) and pseudarils of the dehiscent fruits of Tetragastris and Protium (Burseraceae), are often difficult to process and detach, making seed swallowing the most efficient option to reduce handling time. This is the principal plant strategy promoting endozoochory. Handling time is undoubtedly a crucial factor in fruit feeding in marmosets and tamarins, not merely to maximize energy gain in their high-energy time budgets, but because much of their fruit feeding is in the relatively open canopy level of the forest where, being diurnal and small, they are especially susceptible to predation from raptors. Swallowing seeds in this sense is the nearest thing to cheek pouches. Another possibility promoting fast handling and ingestion of some fruits is competition with other members of the group. The width of the seeds is often very close to that of the width (maximum extension) of the intestine, and it has been argued that large seeds may serve a mechanical function of expelling parasites from the intestine, particularly spiny-headed worms (Prosthenorchis, Acanthocephala) attached to the gut lining and parasitic nematodes (Subulura jacci)—infestations probably come from arthropod prey.
Gums are excreted from tree trunks, roots (buttress and stilt roots), branches, lianas, and fruits of numerous plant species, generally due to damage caused by breakage or wood-boring insects. They often harden to seal the wound. In the case of fruits, notably the bean pods of some species of Parkia (Fabaceae), it would seem that they are produced specifically to attract seed dispersers. They consist mainly of β-linked, complex, non-structural polysaccharides which, because they are β-linked, are indigestible to mammals and as such require microbial fermentation. Gums are composed of fiberthat is soluble in water; their digestion is relatively rapid compared with that of structural fiber, but they slow gastric emptying by increasing the viscosity of the digesta (non-soluble structural fibersuch as cellulose accelerates gastric emptying). Gums are primarily a source of energy and minerals such as calcium, potassium, and magnesium. Gum may be a particularly important source of calcium because insects provide very little. Insects, on the other hand, provide phosphorus that is lacking in gums. The amount of protein (glycoproteins incorporated into the polysaccharide structure) is variable but generally believed to be small, ranging from trace amounts to as much as 9–10% (dry matter content of nitrogen and using a standard conversion value of 6·25 to provide an estimate called “crude protein”). Marmosets and tamarins are hindgut fermenters so it is probable that the small amounts of protein in gum are largely unavailable because they are unlikely to be digested and assimilated in that part of the intestinal tract.
Gums are eaten to a lesser or greater extent by all callitrichids studied so far, but there is an important distinction between tamarins (Saguinus), lion tamarins (Leontopithecus), and Goeldi’s Monkey (Callimico), which can only exploit gums that are readily available (they are sometimes called facultative gummivores), and marmosets (Callithrix and Mico), the Pygmy Marmoset (Cebuella), and the Black-crowned Dwarf Marmoset (Callibella), which have dental and mandibular-cranial adaptations to gouge bark to elicit exudate production, which allows them to eat gums year-round (obligate gummivores). The four marmoset genera are the only monkeys to habitually gouge to obtain exudates. The need to allow for microbial fermentation to breakdown polysaccharides means that their efficient digestion would require a slow passage through the intestine. Estimates of transit time in the different genera of callitrichids, however, indicate an increase that is proportional to body size (and hence gut length) from marmosets to tamarins and lion tamarins. It would be expected that marmosets—specialists in gum feeding—would have relatively longer transit times than tamarins. Only the Pygmy Marmoset has a long transport time for its body size. The intestinal length of the Pygmy Marmoset is about what one would expect compared with other callitrichids and taking into account its body size. The slower passage rate is due to the intestinal contents being slowed down, allowing for prolonged fermentation and more efficient digestion. The reason for the apparent lack of a similar slowdown of digesta in other callitrichids might lie in the conflict in digestive strategies between fruit feeding (fast transit times) and gum feeding (slower transit times). A substantial proportion of the fruit ingested consists of indigestible seeds that pass through the intestinal tract. Marmosets and tamarins are unable to eat, with “full stomachs,” until the seeds are eliminated, hence the need to pass them quickly. This does not affect Pygmy Marmosets as much because they occupy very small home ranges and rarely find fruits to eat. The Common Marmoset, although also highly gummivorous, eats more fruit and does not differ in its passage rate from similar-sized tamarins. It has been found, however, that there is a difference in the passage rate between liquids and solid/particulate matter. Fluids under any circumstances pass through more slowly than particles and smaller particles pass through more slowly than larger particles. There is a possibility that the Common Marmoset has a caecal-colonic separation mechanism, with liquid digesta being retained in the caecum, allowing for enhanced fermentation. Another important possibility concerning the resolution of this conflict between digestion of gum and fruit feeding is that marmosets and tamarins feed on them at different times. Tamarins tend to feed on fruits in the morning and expel the seeds as quickly as they can, and then feed on gums in late afternoon, permitting a long retention time for fermentation through the night. Marmosets tend to have bouts of gum-feeding late in the day before retiring to their sleeping sites, which may be so they can gouge at the holes and stimulate exudation of gum droplets that they harvest the next morning. The prolonged time for fermentation and digestion would be another reason. Despite similar passage times between Common Marmosets and tamarins, marmosets digest gums more efficiently, so there are differences in their digestive strategies that have yet to be clarified. Marmosets have a larger and more complex caecum and colon than tamarins, although their mass-relative intestinal lengths do not differ. The caecum probably serves as a refuge and reservoir for the intestinal bacteria needed for fermentation, especially with the passage of large seeds, giving them an improved ability to maintain large microbial populations in the upper colon.
The primary record of latex consumption among callitrichids is from the Black-tufted-ear Marmoset in the Cerrado of central Brazil. It gouges the trunk of mangaba (Hancornia speciosa, Apocynaceae), which subsequently produces copious quantities of a resinous red latex. The latex is slightly sweet but apparently of little nutritional value. The exocarp of fruits of Couma (Apocynaceae), eaten by a number of callitrichid species, contains a milky-white, sticky latex that is inevitably ingested. Couma latex is tapped from the Couma trunk for industrial use in the manufacture of chewing gum. In both tree species, the latex also is used in folk medicine to remedy diarrhea and intestinal parasite infections.
Nectar provides simple sugars and proteins and is a key resource for a number of callitrichids, particularly tamarins, when fruits are scarce during dry-season months. Nectar from flowers of Combretum assimile (Combretaceae), a small bushy tree, and Quararibea cordata (Bombacaceae), a very tall canopy tree, were important components of the diets of the Pygmy Marmoset, Weddell’s Saddle-back Tamarin, and the Emperor Tamarin at Cocha Cashu, Manu National Park and Biosphere Reserve during the dry season in July–August. Nectar of the red flowers of Symphonia globulifera (Clusiaceae) is an important resource for marmosets (Wied’s Black-tufted-ear and Santarém), tamarins (Geoffroy’s and Spix’s Saddle-back, Mustached, and Black-handed), and lion tamarins (Golden, Golden-headed, and Black). The Atlantic forest plant Mabeafistulifera(Euphorbiaceae) is favoredfor its nectar by the Buffy-headed Marmoset and the Black Lion Tamarin. Nectar of Amazonian species of Mabea is also eaten by the Pygmy Marmoset, saddle-back tamarins (Geoffroy’s and Spix’s), and the Emperor Tamarin. Nectar of the flowers of all these species has been classified as a “keystone” resource during fruit shortages in the dry season. The potential for pollination has been clearly indicated by pollen on the heads and muzzles of all these callitrichids, but Symphonia flowers are destroyed and at least partially eaten and whether or not pollination is effected is unclear. Callitrichids might merely bit off, chew, and spit out Symphonia flowers rather than eating swallowing them.
Consumption of fungi and its importance in the diet of some callitrichid species has only been recognized in recent years. It is an important element in the diet of some populations of the Buffy-tufted-ear and Buffy-headed marmosets and the Black-faced Lion Tamarinin the Atlantic forest in south-eastern Brazil. In the Amazon Basin, fungi are a minor element in the diets of the Mustached, Red-bellied, and Emperor marmosets, but they are a staple in the diet of Goeldi’s Monkey.The saddle-back tamarins, despite forming mixed-species groups with the three species of mustached tamarins and Goeldi’s Monkey, have not been seen eating fungi. The species of fungi eaten by the Buffy-tufted-ear Marmoset have not been identified, but the Buffy-headed Marmoset eats the fruiting bodies, or sporocarps, of two species of ascomycete Mycocitrus (Bionectriaceae) found on bamboo culms (Merostachys and Chusquea). The Black-faced Lion Tamarin eats sporocarps of the ascomycete Mycomalus bambusinus (Clavicipitaceae) on the culms of Chusquea bamboos. Goeldi’s Monkey eats the nearly mature or mature fruiting bodies of five fungal species: three basidiomycete jelly ear fungi, Auricularia auricula, A. delicata, and A. cornea (Auriculariaceae) from rotting trunks and dying tree branches, and two species of ascomycete bamboo fungi, Ascopolyporus polyporoides and A. polychrous (Clavicipitaceae), which produce thin, rubbery sporocarps with a tough outer layer and a clear gelatinous interior on the culms of Guadua weberbaueri (a dominant species in forests of northern Bolivia). The two fungal genera are dispersed differently in the forest; bamboo fungi are singular and sparse throughout the bamboo clumps (one survey indicated 1 clump/20 m2) and jelly ear fungi are found in relatively large numbers in sporadic rotting trunks and branches.
Fungi comprised about 15% of the annual diet of a group of Buffy-tufted-ear Marmosetsin Serra do Mar State Park in São Paulo. Although fungi were eaten throughout the year, consumption was slightly higher (about 25%) in March at the end of the wet season. Fungi were the dietary staple of a group of Buffy-headed Marmosets in Augusto Ruschi Biological Reserve in the montane region of the state of Espírito Santo near the Brazilian coast; fungi accounted for 54–70% of the diet in any given month. Nevertheless, exploitation of fungi does not characterizeentirely the diet of these two marmoset species. Groups of both species studied further inland apparently do not eat fungi at all, concentrating on gums in the dry season when fruit is scarce. Fungi comprised 12·6% of the diet of a group of Black-faced Lion Tamarins studied during eight months on the Island of Superagüi on the coast of the state of Paraná in Brazil. It was the most common food item in the dry season for this species, but mycophagy has not been recorded for the other species of lion tamarins.
In general, fungi have high concentrations of vitamins, minerals, nitrogen, and structural carbohydrates (fiber). This fiber is difficult to digest, and the nitrogen is also largely locked up in the fiberof the cell walls, indigestible spores, or non-protein forms (for example, urea or ammonia). The fiberis mainly in the form of chitin, the main component of insect exoskeletons. Chitin, although a structural carbohydrate, is more easily digested than cellulose or the polysaccharides found in gums. It is not known if callitrichids produce a chitin enzyme (chitinase), and the digestion of chitin otherwise requires fermentation by an intestinal microbe, which in the case of marmosets would occur in the caecum (hindgut fermentation). Goeldi’s Monkeyseat more fungi from 16:00 h to 17:00 h than early in the day, providing a longer period of fermentation and digestion while they rest through the night. The sporocarps eaten by Goeldi’s Monkeys contain mainly fiber (62–83% of the dry matter), along with sugar (2–5·6%), fat (0·9–1·6%) or starch (up to 0·2%), protein (5·5–13·4%), and minerals, especially potassium (1·19–1·68%). Nutritional analysis of the Mycocitrus sporocarps eaten by Buffy-tufted-ear Marmosets revealed that they were high in sugar and fiberbut low in protein, and were similar in their composition not only to Auricularia and Ascopolyporus eaten by Goeldi’s Monkeys but also to some gums that are eaten by other Callithrix species.
Fungi are an essential component diets of groups of Goeldi’s Monkeys in northern Bolivia and the south-western Amazon Basin in Brazil. Fungal sporocarps are eaten throughout the year (about 29% of their feeding time) but especially in the dry season from March to July when fruits are scarce. At this time, they contribute 48–63% to their diet each month; a single individual eats as much 30 g/day. The sympatric saddle-back and mustached tamarinsconcentrate on nectar and gums when fruits are scarce, while Goeldi’s Monkeyincreases its consumption of fungi that they find while foraging for animal prey, low in the understory and near the ground. At times when fruit is abundant, Goeldi’s Monkeystravel with groups of Weddell’s Saddle-back and the Red-bellied Tamarin as much as 89% of the day, but when fruits are scarce, they spend less time together (as little as 13% of the day). Goeldi’s Monkeysconcentrate on bamboo clumps and along river edges where fungi are easily found—areas that are of less interest to tamarins looking for gum and nectar; as such, the “foraging compatibility” of the two species is reduced. Groups of Goeldi’s Monkeys have large home ranges of 100–150 ha, four to five times larger than home ranges of tamarins. Patchy distribution of fungi in time and space (scarce and widespread, low renewal rates) and their low nutritional quality (need to eat a lot) are probably the reasons for this. Gums are consistently available at known sites (for example, a particular tree or clump of Acacia vine). The two marmosets (Buffy-tufted-ear and Buffy-headed) also have large home ranges associated with their propensity to eat fungi. Telling is the finding of a group of Buffy-headed Marmosets in the Caratinga Biological Station (Minas Gerais State, Brazil) that occupies a home range of 35 ha concentrating on gum when fruits are scarce, and a group of Buffy-headed Marmosets in the Augusto Ruschi Biological Reserve that occupies a home range of 138 ha concentrating on fungi when fruits are scarce. These large home ranges affect population densities and are the reason that the three species tend to be rare.
Callitrichids generally spend 20–30% of their ten-hour day of activity searching for small animals, their principal source of protein. Their animal prey is principally Orthoptera—grasshoppers, crickets, and locusts—particularly katydids (Tettigoniidae, including five of its subfamilies), stick grasshoppers (Proscopiidae), lubber grasshoppers (Romaleidae), and raspy and camel crickets Gryllacrididae. They also eat praying mantises (Mantodea, Mantidae), giant cockroaches (Blattodea, Blaberidae), Lepidoptera (larvae), stick insects (Phasmatodea), cicadas (Cicadoidea), weevils (superfamily Curculionoidea) and other beetles, spiders and spiders’ eggs, and scorpions (Scorpiones). Small lizards, frogs, birds, birds’ eggs and nestlings, and snails also are eaten.
Prey foraging patterns, substrates, and techniques differ among callitrichids and are associated with the use of different heights (strata) of the forest, different modes of locomotion, and even differences in the morphology of the hands. Callitrichids are small and agile enough to forage using techniques of stealth—stalk and pounce—for exposed prey on leaves, palm fronds, branches, and tree trunks, catching both sluggish or immobile prey (for example, caterpillars) and large mobile prey (grasshoppers). In contrast, the highly insectivorous squirrel monkeys, being larger and less agile in the catch than callitrichids, specializemore on foliage-gleaning of more sluggish or immobile prey. All species catch prey this way when they can, and it is the principal foraging mode of all saddle-back tamarins, Black-mantled Tamarins, the Golden-mantled Saddle-back Tamarin (Saguinus tripartitus), and lion tamarins. These specializein foraging for hidden prey in specific locations such as knot holes and crevices in tree trunks and branches, curled-up leaves, clumps of leaves, leaf litter, and epiphytes. They are sometimes referred to as “manipulative foragers” as opposed to the “visual search” foragers such as marmosets and mustached tamarins.Hands of the manipulative foragers are adapted to probing in crevices; palms and digits are longer and thinner than in other callitrichids. The non-manipulative, visual-search foragers have hands that are relatively short and wide.
Saddle-back, Black-mantled, and Golden-Mantled Saddle-back tamarins travel and forage below 10 m and mostly at heights below 5 m, even going to the ground to pick through leaf litter, especially, for example, to chase a grasshopper that dropped from the foliage above. The lion tamarins occupy primarily the forest canopy. The Golden-headed Lion Tamarin, for example, forages mostly at about 12–20 m in the middle to upper canopy, where it hunts in large epiphytic bromeliads, palm crowns, and dense tangles of lianas. By comparison, the sympatric Wied’s Black-tufted-ear Marmoset forages mostly in the lower canopy and understory at 6–13 m above the ground.
Saddle-back tamarins, the Pygmy Marmoset, and Goeldi’s Monkey travel and forage in the understory 5 m or less above the ground, and because the vegetative structure is mostly vertical, much of their locomotion can be classified as “vertical clinging and leaping.” They regularly use large and medium-sized vertical substrates such as tree trunks and large vines, in contrast to the larger mustached tamarins(Mustached, Red-bellied, and Emperor). Visual-search foragers such as the mustached tamarinstravel and forage in the middle and lower canopies, from about 10 m to 15–20 m above the ground, in a branchy environment with more horizontal and oblique substrates, and as such, they are mainly quadrupedal runners and jumpers. Their leaping is more often between branches, rather than between vertical supports. Lion tamarins, foraging mainly in the canopy particularly among large tank bromeliads, are also predominantly quadrupedal runners and jumpers. Marmosets (Mico and Callithrix) follow army ants when swarms pass through a group’s home range; they pick off prey flushed in the leaf litter at the head of the swarm.
Callitrichids are unusual among primates and even among mammals in a number of aspects of their mating and reproduction. They have a variable mating system, ranging from monogamy to polygyny and polyandry, and even polygynandry (two or more males mate with two or more females) associated with groups of 2–20 individuals with, accordingly, variable compositions of sexually mature adults. Except for Callimico, which has single offspring,they have multiple births (typically fraternal twins, sometimes singletons, and in captivity sometimes triplets and even quadruplets). Although there may be more than one adult female in a group, generally only one of them breeds. Goeldi’s Monkey is an exception, often having two breeding females in a group, and Atlantic forest marmosets, which form the largest groups of the callitrichids, occasionally have two, or even three, breeding females in the same group, although infant survival is highest for one, the dominant breeding female, and poor for the offspring of the subordinate females. Infants are carried by other group members and are given food items during weaning and as juveniles. Provisioning of weaned young is a significant aspect of the cooperative breeding system of callitrichids. Juveniles receive a substantial proportion of their food from all adult group members, whereas juveniles of most other primates receive little from their mother and generally only through scrounging. The father may carry the infants from the day of their birth in all species except for the lion tamarins and Goeldi’s Monkey where the mother generally carries them exclusively until they are about three weeks old. After becoming an adult, offspring tend to remain in the group for a year or two and help care for their younger siblings.
Breeding female callitrichids have a post-partum estrus and are able to conceive again shortly (as little as 2–4 weeks) after giving birth. Callitrichids do not menstruate. Sexual behavior occurs at any time during the ovarian cycle and even during pregnancy, but it tends to be more frequent during the periovulatory period. Marmosets and Callimico generally breed twice a year, but tamarins and lion tamarins breed just once a year. Gestationperiod ranges from 125–129 days in lion tamarins, 140–145 days in marmosets, 145–150 days in saddle-back tamarins, mustached tamarins,and Goeldi’s Monkeyto a maximum of 183 days in the Cotton-top Tamarin. Growth and maturation are rapid, infants are independent after about fivemonths, females are capable of ovulation at 12–17 months, and males begin producing sperm by 13–18 months, siring infants by 15–25 months. All these aspects result in a very high reproductive potential that is not achieved by any other haplorrhine primate.
Although the reproductive potential of any one individual is high, it is not always fully realized because of the dominant female’s suppression of reproductive activity in her daughters and other subordinate females in the group. This results in the functional sex ratio biased toward males and implies competition among females and among males for breeding opportunities; there is delayed breeding and rank-related variance for both sexes. In lion tamarins, daughters usually ovulate normally and reproductive suppression is behavioral.When subordinates do breed, the offspring commonly survive. In tamarins, daughters living in the group where they were born generally fail to ovulate, whereas in marmosets, this is the case for only about 50% of the females (some show ovarian cycling, some do not). In tamarins, subordinate females rarely breed, and infant survival is always very poor. Groups of the Pygmy Marmoset and Goeldi’s Monkey are always small, and daughters ovulate but are not allowed to breed by behavioral suppression. In the Pygmy Marmosets, only one female breeds in each group, but in Goeldi’s Monkeys about 33–50% of groups have two breeding females, both successfully raising single offspring.
Reproductive suppression, behavioralor physiological or both, is never quite perfect, and when there is more than one female breeding in a group, it is possible that the dominant female is near the end of her reproductive life, that there is a challenge to her dominance under way, or, conceivably, that a breeding female may simply allow her daughter to breed when food and availability of infant carriers are sufficient. Incest avoidance means that daughters do not mate with their fathers or brothers, but when an unrelated adult male enters the group, this may activate a daughter’s sexual activity. If she is not behaviorallysubordinate to the mother, this can result in more than one breeding female in the group. Infant survival drops with increasing parturitions, suggesting that there may be age or parturition effects on lactation. Aging females may lose their ability to suppress breeding in subordinates. Captive female Common Marmosets start breeding well past sexual maturity and stop breeding at 8–9 years old. The entry of a strange, unrelated male into the group can sometimes cause daughters to become sexually active and even to take over from their mother as the breeding female. Under any circumstances, all callitrichid females seem to be able to control the breeding of other females in the group. When dominant and subordinate females breed in the same group, the subordinate’s infants generally have a lower survival rate. Cases have been reported of the dominant female killing the subordinate’s infants. Perhaps because of this, subordinate breeding females carry their young exclusively for up to ten days after the birth (longer than dominant females). About one-quarter of all groups of Golden Lion Tamarins have two pregnant females, but only those groups with new, immigrant males at the time of conception successfully reared their offspring. Successful simultaneous rearing of two litters in groups of Common Marmosetsis possible when their births are separated by more than a month.
After callitrichids achieve sexual maturity, females have to search for reproductive opportunities. The options are to stay in their natal group and eventually become the dominant female (taking over from her mother and perhaps competing also with siblings), disperse to another group where there are improved opportunities to breed, or disperse and form a new group with one or more males from another group. All strategies have been observed in the wild.
The reason for singular breeding (just one breeding female in group) rather than plural breeding (two or more females breeding in a group) in callitrichids probably results from the need for group members to help in the care of the offspring. In some cases it has been found that infant survival is higher in larger groups (more helpers) than in smaller groups, but there is evidently an upper limit of four or five helpers, above which further group members will be superfluous. A second breeding female, however, would compete for helpers. The reason why breeding females need helpers is related to their high fecundity; callitrichid neonates are large, generally 8–10% of the mother’s weight and, with the occurrence of a fertile post-partum estrus, the female is frequently pregnant while lactating. How she can command the help of other group members (alloparental behavior) is believed to arise from a number of factors, including advantages to helpers not just the breeding female. Helpers improve their parental skills, alloparental behavior may increase the likelihood that they will achieve a breeding position, males may increase their access to the breeding female (courtship), and individuals may increase their inclusive fitness by improving the survival of their siblings. The father’s care is easier to explain in terms of nurturing his own infants, and when the female mates with more than one male (polyandry), there is the element of paternal uncertainty that can motivate the help of more than one male in carrying and provisioning the young.
Twinning is evidently a specialized, not a primitive, condition in callitrichids. There is a general rule that primates have a ratio of 2:1 between the number of teats and the number of offspring at birth. All haplorrhines have two teats and single births, except for callitrichids with two teats and twin births. They have a simplex uterus, believed to be ancestral in simians and associated with single births, and an invasive haemochorial placentation. Callitrichid twins in this simplex uterus share a common placental circulation, even exchanging cells from a few days after implantation (chimaerism). When this occurs in cattle and the sexes of the fetuses are different, the female offspring is sterile and imperfectly developed (so-called “intersex freemartins”). This is because in ungulates, as in primates, testicular hormones organizeneural development of sexual behavior in the developing male brain before birth. The exchange of hormones between fetusesof different sexes might also be expected to cause developmental problems in calltrichids, but females born as co-twins with males develop normally. Callitrichids have overcome the problem of neonatal androgenization by delaying some aspects of sexual differentiation (neural mechanisms controlling reproductive behavior) until after birth. Unlike other primates, male callitrichids are exposed to higher circulating concentrations of testosterone than females only 50–80 days after birth.
All callitrichid genera, except for lion tamarins, have longer gestation periods than would be expected from their body size. Lion tamarins have a gestation of 125–129 days, which is the shortest of any of the monkeys, but it is about as long as would be expected considering its size. In all mammals, there is an initial period in gestation, called the “lag phase,” in gestation when growth of the fetusis slow. The lag phase typically increases in proportion to the gestation length. The unusually prolonged gestation of callitrichids (other than lion tamarins) is due to unusually prolonged lag phases—a unique trait of callitrichids among the primates. According to their body weights, the Pygmy Marmoset should have a gestation length of 105 days but the actual period is 137 days. Likewise, the Cotton-top Tamarin has gestation period of about 183 days (the longest of the callitrichids), when its body weight would predict 125 days. Goeldi’s Monkey also has a long lag phase; it has a gestation period of 150 days, but its body size would predict 129 days, similar to that of lion tamarins that are just slightly larger. Extension of gestation beyond that expected based on body size, therefore, ranges from four to six weeks. The reason for this extended lag phase may lie in the fact that callitrichids have a post-partum estrus—a mechanism by which females can conceive shortly after giving birth while minimizing their energy costs at a time when they are carrying the young (albeit with the help of other group members) and lactating. In a number of callitrichid species, females can be pregnant and yet fail to give birth, indicating abortion or reabsorption of the fetuses.This is probably,a mechanism to provide for readiness and an efficient response in breeding when there is a degree of unpredictability in seasonal environments. Marmosets and Callimico generally breed twice a year, and Saguinus does so only occasionally. The prolonged lag phase may be important in minimizing the energetic burden of the developing fetusor fetuses andduring lactation and infant carrying, while maximizing reproductive rate in response to favorableconditions as the pregnancy continues. If conditions become unfavorable, the female is evidently able to terminate the pregnancy. The lack of a prolonged lag phase in lion tamarins may well be due to their occupation of an adaptive zone of mature lowland forest that has more predictable (albeit seasonal in some areas) food resources during the year and from year to year.
Movements, Home range and Social organization
Marmosets and tamarins live in social groups of up to 20 or so individuals. The Pygmy Marmoset tends to live in stable, small groups of 2–9 individuals, with one or two adult females (only one breeds) and one or two adult males, and offspring of up to four successive litters. Marmosets (Callithrix and Mico) tend to live in larger groups (up to 20 members) than the tamarins (maximum recorded is 13 members), lion tamarins (up to ten members) and Goeldi’s Monkey (4–12 members). This is believed be due to their tree gouging and gum feeding, which guarantees food during times of fruit shortage, when other species rely opportunistically on nectar and gums as their availability allows and, consequentially, breeding twice a year, resulting in greater recruitment. There is evidence to suggest that breeding female tamarins may become pregnant a second time in the year but spontaneously abort when conditions are unfavorable.Although they breed twice a year, the limiting resource for the Pygmy Marmoset is the availability of one principal and some secondary sources of gums and abundance of insects in a very small home range. Resource and habitat constraints might set the upper limits of group size. The same is true of Goeldi’s Monkey with regard to the availability of fungi. Lion tamarins and tamarins have larger home ranges but a lower annual recruitment than marmosets. All species can have groups with supernumerary adults, a hierarchy of a dominant male and female and subordinates, young, and peripheral group members, ranking low in terms of social interactions such as mutual grooming, and often immigrants or soon-to-be emigrants.
Home-range sizes vary from less than 1 ha for the Pygmy Marmoset to 150 ha for Goeldi’s Monkey and more than 300 ha for Black and Black-faced lion tamarins. The distances they travel vary accordingly: Pygmy Marmosets travel 250–300 m/day; the more exudativorous Atlantic forest marmosets, occupying home ranges of 0·7–30 ha, generally travel 900–1200 m/day; tamarins, with home ranges of 40–60 ha, generally travel 1000–1800 m/day; and lion tamarins and Goeldi’s Monkeys, with home ranges exceeding 100 ha and in some cases as large as 300 ha, travel up to 3000 m/day. Callitrichid groups are territorial, and group encounters are characterized by frequent long calling, displays, scent marking, agitated behavior, chasing, and sometimes physical aggression. Territorial defenseindicates protection of stable and key resources, and that seasonal variations in the use of space by callitrichids tend to be less pronounced than in, for example, the less territorial capuchin and squirrel monkeys. The long fruiting periods of the major plant species used by callitrichids probably buffer against fluctuations in resource availability. While home-range limits can be clearly identified, there is often considerable overlap between groups, regularly 10–20%. Groups of Black-faced Lion Tamarins occupy home ranges of up 300 ha that can entirely overlap with other groups; the groups rarely meet, and defenseis evidently not feasible (or worthwhile) for such a large area; instead, they practice a form of time sharing. Intergroup encounters are also seen as a mechanism by which non-breeding adult group members can appraise opportunities for dispersal, and, in Common Marmosets at least, females can mate with males from neighboringgroups. Relations among neighboringgroups can vary in character from evidently friendly (groups merge and forage and travel together for a awhile without any agitation or display), to subordinate (for example, a group waits until a neighboringgroup has left a fruiting tree), to extremely agitated (chasing and calling, which can continue intermittently, with sporadic bursts of agitation, long-calling and chasing, for hours). In the first case (friendly), groups probably have members that are kin.
Both sexes of callitrichids disperse, with individuals leaving their natal group and entering another, or joining up with other dispersing individuals (for example, a female joining two males) to form a new group and new home range. Groups are generally quite stable with gradual changes in composition from deaths, births, emigration, and immigration. Very dynamic and unstable groups are found in areas where human activities have increased the abundance and changed the spatial and temporal availability of food resources (often accompanied by destruction of their natural environment). Small mosaics of scrubby second growth with scattered fruit trees in backyards or as plantations can result in high and strongly fluctuating population densities with unstable groups that increase rapidly in size and then dismantle with episodes of low infant survival and high adult mortality due to disease. Their social organization, which has evolved to adapt to certain predictable patterns of resource availability in time and space, appears to breakdown these circumstances.
Secondary growth and forest in succession are important for marmosets and tamarins. These habitats arise from tree falls and abiotic conditions (for example, soils, drainage) that tend to maintain relatively open canopies and densely vegetated understories. In undisturbed areas, Pygmy Marmosets depend on inundated forest.Lion tamarins are essentially adapted to mature forest, and Goeldi’s Monkey occupies stream edge and bamboo forest. One of the keys to understanding the evolution of their social organization and reproductive behavior lies in an understanding of these habitats in terms of successional stages, floristic composition, and renewal rates, and the distribution, seasonality, and abundance of fruit, gums, nectar, and animal prey in them.
The second major determinant of social organization of callitrichids is undoubtedly predation. Being small, social, and diurnal, they are prey to a wide array of predators, but their sociality and agility and a preference for dense vegetation in the lowest layers of the forest are their key defenses.They are constantly alert and, on perceiving a threat, give alarm calls that result in the group moving rapidly into cover in the understory and freezing. Known and potential predators of callitrichids include snakes, cats, buzzards, falcons, hawks, and eagles. The Tayra (Eira barbara), a large mustelid, is often seen near callitrichid groups, and they are always mobbed when seen. The cats include the Ocelot (Leopardus pardalis), the Oncilla (L. tigrinus), the Margay (L. wiedii), the Jaguarundi (Puma yagouaroundi), the Jaguar (Panthera onca), and the Puma (Puma concolor). Raptors, toucans (Ramphastos), vultures, and other larger birds, flying overhead or nearby, always cause a spate of alarm calls. Accipitrid and falconid species noted by field researchers as predators include the harpy eagle (Harpia harpyja), the ornate hawk-eagle (Spizaetus ornatus), the Guiana crested eagle (Morphnus guianensis), the black-and-white hawk-eagle (S. melanoleucus), the bicoloredhawk (Accipiter bicolor), the slate-coloredhawk (Leucopternis schistacea), buzzards (Buteo and Buteogallus), the crested caracara(Polyborus plancus), the barred forest-falcon(Micrastur ruficollis), and the white-tailed kite(Elanurus leucurus). Callitrichids will mob snakes. Recorded cases include Illiger’s Saddle-back Tamarin mobbing an emerald tree boa (Corallus caninus), high up in a tree, and a bushmaster (Lachesis muta), resting on the ground between the stilt roots of a tree. A mixed-species group of Geoffroy’s Saddle-back Tamarins and Mustached Tamarinsmobbed and bit a boa constrictor (Boa constrictor) evidently causing it to release a subadult Mustached Tamarin that it had caught. An anaconda (Eunectes murinus) caught an adult female in a group of Mustached Tamarinswhen it crossed a stream.
Studies of captive groups of Geoffroy’s Tufted-ear Marmosets have provided interesting insights concerning their vigilance for predators. Exposure to a predator just prior to entering their sleeping site in the late afternoon affects their behavior the next day. Showing the group a snake before it retires made them more vigilant the next morning, and they delayed going to the ground to forage longer than usual. Marmosets are naturally vigilant, but when focusing on their immediate surroundings in search of prey, they are more easily startled and regularly interrupt their foraging to make prolonged sweeping scans to check for predators. Perhaps as a perceived increase in vulnerability while foraging, individuals carrying infants never foraged. Perceiving a non-imminent threat such as a perched owl, vigilance increased in the group as a whole, and foraging and play, for example, were reduced. All members of the group took turns in monitoring the threat. Marmosets also react strongly to the calls of raptors. Taped calls of a red-tailed hawk(Buteo jamaicensis) elicited startle reactions, alarm calls, and freezing, and disrupted the group’s activities. For ten minutes, they monitored the perceived direction from which call came and minimized their movements for about 30 minutes before resuming their previous activities.
In the wild, raptor attacks on Weddell’s Saddle-back Tamarins in Manu National Park and Biosphere Reserve occurred weekly, and mixed groups of Mustached Tamarins and Geoffroy’s Saddle-back Tamarins at the Rio Blanco Research Station emitted 0·3–0·5 avian predator alarms/hour. A mixed-species group of the Ávila Pires’ Saddle-back Tamarinand the Red-cap MustachedTamarin at Urucú, Brazil suffered attacks from raptors about once every nine days. Prolonged vigilance following encounters with predators has also been noted in the wild. After an attack by an ornate hawk-eagle, a group of MustachedTamarins feeding in the exposed crown of a tree in the early morning (07:50 h) literally fell out of the tree in their panic; they remained quiet, resting not even grooming, for about three hours. For the remainder of the day and on subsequent days, they travelled and foraged at lower heights and doubled their normal rate of alarm calling.
Black-collared hawks (Busarellus nigricollis) and double-toothed kites (Harpagus bidentatus) are known to accompany callitrichid groups to catch flushing insects, particularly cicadas at certain times of the year. The presence of the kites, which follow groups for up to two hours at a time, is generally ignored, but occasional attempts to drive off a kite results in alarm calling when it flies up. Tamarins showed an overall increase in their rate of alarm calling when kites followed them.
Sleeping sites chosen by marmosets and tamarins are evidently places of concealment—in tree holes and dense vegetation—generally higher above the ground than their customary levels of traveling, resting, and foraging. When using more exposed sleeping sites (such as in forks and crotches of trees), difficulty of access or the impossibility of being surprised no doubt determine choice. Although owls are not believed to primary predators of callitrichids, at night it may well be that scansorial predators such as small cats, Tayra, coatis, and snakes demand vigilance and security. Quiet and stealthy behaviors while travelling to and entering sleeping sites are seen in all callitrichid species and undoubtedly signify vigilance and care to avoid predators.
Communal infant carrying and provisioning, allogrooming and low rates of aggression among group members, alarm calling, sentinel behavior noted for some species (for example, Weddell’s Saddle-back Tamarins and Geoffroy’s Tamarins), mobbing, and even attacking predators are behaviorsthat signal the extremely cooperative nature of callitrichid social groups. N. Caine, a researcher of tamarin social behavior, has argued cogently that predation has been a major selective force for an increased reproductive rate, flexibility in the mating system, and cooperative breeding and sociality among callitrichids.
Relationship with Humans
In the wild, marmosets and tamarins can often be seen around cultivated plots, gardens, and backyards and in scrubby second growth near houses and villages. As long as they are not persecuted, they can thrive in these areas, eating fruit from cultivated trees such as mangos, cashew, bananas, and figs. They also use secondary growth produced by logging and road construction. Callitrichids are generally not hunted for food because they are too small. They are, however, favoredas pets because they are small, attractive, active, and agile. There is a constant trade in callitrichidson a local and even national scale within the South American countries where they occur. They are often sold as pets, along with bushmeat, by the roadside (more so in the past than today). In north-eastern Brazil, infant Common Marmosets are frequently purchased by truck drivers traveling south, who subsequently let them go on the roadside when they tire of them. This has resulted in widespread invasion and hybridization outside of their range south of the Rio São Francisco and in south-eastern Brazil where they are possibly displacing less robust species (Buffy-tufted-ear and Buffy-headed marmosets). In the past, at least, they were taken from the wild and exported overseas as pets and experimental animals, and for exhibition in zoos.
The burgeoning biomedical and pharmaceutical industries in the 1960s believed strongly in the value of these primates for experimentation and in drug and toxicological testing. Their closeness to humans, the fact they are small (can be kept in small cages in large numbers) but large enough for routine surgery and serological monitoring, low maintenance costs, and being prolific breeders (twins and even triplets when well fed) with a short generation time made them very useful laboratory animals. They adapted well to laboratory environments, and some species proved susceptible to oncogenic viruses and human infectious hepatitis. The establishment of captive colonies, principally of tamarins in the USA and Common Marmosets in Europe, has resulted in numerous lines of research in immunology, teratology (study of abnormalities in physiological development), cancer, dentistry, perception and cognition, behavior and neuroendocrinology, and biomedicine in general. They were also widely used for routine drug testing. The development of placental vascular anastomoses leading to hemopoietic chimaerism and immunological tolerance between the fraternal twins of marmosets and tamarins (unique among mammals) makes them important models for immunology research.
The principal species involved in biomedical and laboratory research are the Common Marmoset (exported from Brazil), the Cotton-top Tamarin (Colombia), and the saddle-back and Black-mantled tamarins (Colombia and Peru). Mustached Tamarins and Red-bellied Tamarins were particularly valued as a model for hepatitis research (to replace chimpanzees) and were taken in large numbers from the wild in Bolivia, Brazil, and Peru, although the former adapted poorly to captivity. Tamarins overall were found to be suitable models in immunology, virology, and oncology. The Cotton-top Tamarin has been used extensively as a research model for colitis and colon cancer. Of particular interest, and generating considerable research, was the discovery of the physiological reproductive suppression of subordinate females by dominant females; this has been studied extensively with the hope advancing new and better contraceptives for humans.
From the 1960sto the mid-1970s, large numbers of marmosets and tamarins were exported from the so-called “habitat countries,” legally and illegally. Official import records to the USAfrom 1968 to 1972 recorded the entry of 17 species of callitrichids, including more than 1000 MustachedTamarins, 13,711 Cotton-top Tamarins, and 9135 Black-mantled Tamarins. Imports between 1976 and 1980, included 4296 Red-bellied Tamarins, 1683 MustachedTamarins, and 1669 Cotton-top Tamarins. With the prohibition of primate exports imposed by Colombia, Peru, and Brazil between 1976 and 1979, breeding colonies were established to maintain the demand for these animals, and research on husbandry and maintenance became a priority; for many years, the only focus was on breeding and production. In turn, researchers recognized that physiological effects of stress and even disruption of such basic, but complex, phenomena as physiological and biochemical circadian (daily) rhythms could have major influences on the outcomes of experimentation and drug testing. There also were concerns about the need for humane captive conditions and appropriate social and physical environments. As a result, the pharmaceutical industry and researchers came together to improve protocols for captive care and worked to create an information exchange forum, the European Marmoset Research Group in 1992 and the Marmoset Research Group of the Americas ten years later. These groups have resulted in a considerable increase in research on the needs and appropriate husbandry and maintenance regimes and have stimulated considerable progress concerning care and welfare of captive marmosets and tamarins in laboratories, industrial settings, and zoos.
Perhaps unrecognized but important is the role of callitrichids as seed dispersers and pollinators that promote secondary succession in disturbed and destroyed forests. This is of particular note in many regions of the Amazon Basin and Atlantic forest and northern Colombia where restoration and regeneration of tree cover are needed to provide refuge and connectivity among forest patches and promote water and soil conservation. There are instances of successful local and regional conservation programsusing callitrichids as “flagship species” to provide a focus, or a hook, for promoting biodiversity conservation and protecting forests and landscapes, while at the same time improving the livelihood and well-being of local communities. Notable examples have been programsfor lion tamarins in Brazil, the Cotton-top Tamarin in Colombia, and the Pygmy Marmoset in Ecuador.
Status and Conservation
In most cases, the principal threat to marmosets and tamarins in the wild is deforestation, combined with their relatively restricted or very small geographic ranges. In general, their affinity to successional, disturbed, secondary forest means that they can be found, even in high numbers, in areas of degraded forest around, for example, cultivated plots and backyard gardens and near houses, often benefitting from cultivated fruit trees. When left alone, some of the hardier species of marmosets and tamarins can even be found in parks and remnant forest lots in towns and cities. Hunting is generally not a serious threat until their populations become severely reduced and fragmented. Fourteen callitrichids are threatened, with two listed as Critically Endangered on The IUCN Red List—the Cotton-top Tamarin in Colombia and the Black-faced Lion Tamarin in south-eastern Brazil. Long-term and intensive occupation by humans in northern Colombia and south-eastern Brazil has resulted in the near demise of the Cotton-top Tamarin, the White-footed Tamarin, and the four lion tamarin species. Major conservation programsfor the wild populations combined with captive breeding programs in collaboration with zoos have brought or are bringing these six species back from the brink of extinction. Populations of all but the Golden-headed Lion Tamarin (the most populous of the four species) are small but stable or timorously increasing. The Black Lion Tamarin and the Golden Lion Tamarin were recently upgraded on The IUCN Red List from Critically Endangered to Endangered as a result of these efforts, and today, conservation action focuses on reforestation and the constant monitoring and management of the few remaining populations; both species number less than 2000 in small, fragmented populations. Less than 400 Black-faced Lion Tamarins occupy a tiny range, which is largely protected, but their survival requires constant vigilance. The lion tamarins have benefitted from extraordinary, concerted, and long-term efforts on their conservation by the Brazilian government, national and international non-governmental conservation organizations, universities and zoological gardens.
The two Colombian species of tamarins face continuing and rabid pressure from development and deforestation within their geographic ranges; numbers are down to very few thousands and continue to decline. Unlike the lion tamarins, they have minimal and severely degraded protected areas as refuges. Both are now benefitting from in-situ conservation programs, working especially with government and local communities to protect critical habitat. The Pied Tamarin is disadvantaged by having a tiny range, at the heart of which is the capital of the state of Amazonas, now a sprawling modern city with a prosperous industrial district and fomenting urban and rural development including cattle ranching, plantations, highway construction (a bridge now spans the mighty Rio Negro), and one of the largest hydroelectric dams in the world. The Pied Tamarin is certainly the most threatened of the Amazonian callitrichids, and it is also being displaced by a spreading population of the Midas Tamarin.
Two marmosets in south-eastern Brazil, the Buffy-headed Marmoset and Buffy-tufted-ear Marmoset, are also threatened; the former more so because its range is smaller and its forests are severely fragmented. The Buffy-tufted-ear Marmoset occurs in wider expanses of continuous forest, but both species are confronting displacement by introduced and invasive Common Marmosets and Black-tufted-ear Marmosets. The Black-handed Tamarin is threatened because of the rapid, massive, and widespread destruction of its forests over the last 20 years in the eastern limits of the Amazon in the state of Pará. The landscape in the region has changed from a forest with intermittent deforestation to a bleak landscape of forest fragments. Three Amazonian marmosets—the Black-crowned Dwarf Marmoset, Rondon’s Marmoset, and the Golden-white Bare-ear Marmoset (Mico leucippe)—are considered Vulnerable because of their minuscule geographic distributions in regions facing ongoing forest loss for urbanization and industrial-scale plantations, particularly of soy beans.
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